The rat Lux Actuating Search Task (LAST) and effects of sleep deprivation on task reversal performance

Abstract

Sleep deprivation (SD) causes significant deficits in multiple aspects of cognition, including sustained attention and working memory. Investigating the neural processes underpinning these cognitive losses has proven challenging due to the confounds of current animal tasks; many employ appetitive or aversive stimuli to motivate behavior, while others lack task complexity that translates to human studies of executive function. We established the Lux Actuating Search Task (LAST) to circumvent these issues. The LAST is performed in a circular, open-field arena that requires rats to find an unmarked, quasi-randomly positioned target. Constant low-level floor vibrations motivate ambulation, while light intensity (determined by the rodent's proximity to the target destination) provides continuous visual feedback. The task has two paradigms that differ based on the relationship between the light intensity and target proximity: the Low Lux Target (LLT) paradigm and the High Lux Target paradigm (HLT). In this study, on days 1-6, the rats completed nine trials per day on one of the two paradigms. On day 7, the rats were either sleep deprived by gentle handling or were left undisturbed before undertaking the opposite (reversal) paradigm on days 7-9. Our results showed that SD significantly impeded the ability of Long Evans rats to learn the reversal paradigm, as indicated by increased times to target and increased failure percentages compared to rats whose sleep was undisturbed. Rats also showed reduced learning with the HLT paradigm, as the initial task or as the reversal task, likely due to the rodents' photophobia limiting their motivation to navigate toward a bright light, which is required to succeed.

Keywords: Attention; Cognition; Cognitive flexibility; Light; Reversal learning; Rodent models; Sleep loss.

Fig. 1

Schematic of the LAST arena and insertion/target map. The open field arena is encircled by an acrylic wall, with two LED SMD 5050-300-IR infrared Tri-Chip flexible LED strips (LEDLightsWorld) mounted around the arena perimeter (B). There are also four, 45 mm electric rotary motors (model 345–400; Precision Microdrives) located at the base of each leg of the arena platform. The apparatus also includes a Manta G-201 digital camera with an infrared filter (Allied Vision), two TB6612FNG dual motor driver carriers (Pololu), a chipKIT WF32 microcontroller (Digilent), and a computer with LabVIEW software and a PCIe-6341 multifunction I/O card (National Instruments). (B) The LAST arena insertion points (N=North, W=West, E = East, and S=South) are shown with their associated, equidistant target destinations (N1-3 for entry point N, W1-3 for entry point W, S1-3 for entry point S, E1-3 for entry point E).

Fig. 2

Light intensity gradients for the LLT and HLT paradigms. A schematic of the ambient light intensity produced for any given XY coordinate of rat position in the open field arena with light intensity either decreasing (A; LLT) or increasing (C; HLT) as the rat approaches the target (red circle). The green circle identifies the pre-determined entry location. The LAST light intensities are shown as mean (+/-SEM) functions of the distances from the target for the LLT (B) and HLT (D) paradigms. Lux was measured with a luminometer (sampled in triplicate), while a stationary object was incrementally moved from the outer edge of a target destination. . (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3

LAST performance for rats in the LLT – HLT reversal and HLT – LLT reversal groups. Data are plotted as group means ± SEM for all rats (solid gray) on days 1–6 (pre-reversal days), and for the CONT (gray stripes) and SD (black stripes) groups on days 7–9 (post-reversal days). Between-day comparisons between days 1–6 included all rats (not differentiated by group) and between-day comparisons between days 6–9 were made within-group (CONT and SD differentiated). Statistically significant between-day differences are indicated by lines and asterisks. Between-group comparisons were performed for days 7–9. Statistically significant within-day differences between the CONT and SD groups are indicated by asterisks alone. *p < 0.05, **p < 0.01. ***p < 0.001.

Fig. 4

Representative LAST performance traces for rats in the LLT – HLT and HLT – LLT reversal groups with and without sleep deprivation. Path traces of trials 6–9 of sessions 1, 6 and 7 (S1, S6 and S7, respectively) from a rat in each of the four groups (A–D). The three session traces are aligned on target destination (blue circles) and traces depict position, direction (arrows) and speed (color). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)