Feeder Approach between Trials Is Increased by Uncertainty and Affects Subsequent Choices

Abstract

Animals quickly learn to approach sources of food. Here, we report on a form of approach in which rats made volitional orofacial contact with inactive feeders between trials of a self-paced operant task. This extraneous feeder sampling (EFS) was never reinforced and therefore imposed an opportunity and effort cost. EFS decreased during initial training but persisted thereafter. The relative rate of EFS to operant responding increased with novel changes to the operant chamber, reward devaluation by prefeeding, or lesions to the dorsolateral striatum. We speculate that this may function to increase exploration when the task is uncertain (early in learning or introduction of novel apparatus components), when the opportunity cost is low, or when the learned sensorimotor solution is compromised. Moreover, EFS strongly affected subsequent choices by triggering a lose-shift response away from the sampled feeder, even though it occurred outside of the trial context. This indicates that at least some behaviors occurring between trials impact future behaviors and should be considered in decision-making studies.

Lose-Shift Responding in Humans Is Promoted by Increased Cognitive Load

“…WSLS responding decreases with longer ITIs in rhesus monkeys (Deets, 1970 ) and in pigeons (Rayburn-Reeves et al, 2013 ). We did not find such a temporal relationship with win-stay in the present data, providing evidence supporting the hypothesis that win-stay and lose-shift are mediated by different neural mechanisms (Skelin et al, 2014 ; Gruber and Thapa, 2016 ; Gruber et al, 2017 ). We can only speculate on the information encoded by the decaying memory trace, but we suspect it is an inhibition of the reward position rather than an explicit representation of the reward omission.…”

“…We instead propose that lose-shift is mediated by sensorimotor systems, including the putamen in primates or LS in rodents. This is consistent with lesion data in rats (Skelin et al, 2014 ; Gruber et al, 2017 ), and impairments in a similar task (Rock-Paper-Scissors) in human patients with damage to the putamen (Danckert et al, 2012 ). Furthermore, it provides a parsimonious explanation for the increase in lose-shift in adults under load: the normal suppression of sensorimotor control by PFC (Jahanshahi et al, 1998 ; Knoch et al, 2005 ) is disrupted by the subtraction task, thereby unmasking lose-shift behavior mediated by sensorimotor system.…”

“…We have recently discovered (Skelin et al, 2014 ; Gruber et al, 2017 ) that lose-shift responding in rats depends on the lateral striatum (LS), a sensorimotor region of the striatum homologous to the putamen in primates (Johnston et al, 1990 ; Voorn et al, 2004 ; Balleine and O’Doherty, 2009 ). The PFC normally inhibits the behavioral control exerted by sensorimotor systems, which includes the expression of habits (Jahanshahi et al, 1998 , 2000 ; Knoch et al, 2005 ).…”

Cannabis use is associated with sexually dimorphic changes in executive control of visuospatial decision-making

“…Although the win-stay and lose-shift are complementary response strategies, they are anatomically disassociated among goal-directed and sensorimotor systems. Lesions to the rodent lateral striatum (LS), which is homologous to the human putamen and essential for sensorimotor control (Parent and Hazrati, 1995 ), disrupt lose-shift responding but not win-stay (Skelin et al, 2014 ; Gruber et al, 2017 ; Thapa and Gruber, 2018 ). A similar shifting deficit has been observed in humans with damage to putamen or insula (Danckert et al, 2011 ).…”

“…A similar shifting deficit has been observed in humans with damage to putamen or insula (Danckert et al, 2011 ). Conversely, lesions of the rodent ventromedial striatum (VS), a key structure in goal-directed control that receives inputs from prefrontal cortex (Voorn et al, 2004 ), disrupts win-stay but not lose-shift responding (Gruber et al, 2017 ). Several other behavioral features in rodents and humans support this anatomical disassociation.…”