Developmental exposure to concentrated ambient particles and preference for immediate reward in mice

Abstract

Background: Recent epidemiological studies indicate negative associations between a diverse group of air pollutants and cognitive functioning in children and adults, and aspects of attention deficit in children. Neuroinflammation and oxidative stress are two putative biological mechanisms by which air pollutants may adversely affect the brain.

Objectives: We sought to determine whether exposure to concentrated ambient particulate matter (CAPS) during the first 2 weeks of life, alone or again in adulthood, could alter responding for delayed reward, a critical component of human decision making. Greater preference for immediate reward has been implicated as a component of several psychiatric disorders, addiction, obesity, and attention deficit.

Methods: C57BL/6J mice were exposed to ultrafine particles (< 100 nm in aerodynamic diameter; CAPS) using the Harvard University Concentrated Ambient Particle System (HUCAPS) or filtered air in the postnatal period (days 4-7 and 10-13) with and without adult exposure over days 56-60. In adulthood, delay behavior was assessed using a fixed-ratio waiting-for-reward (FR wait) paradigm in which 25 responses (FR25) were required to initiate the waiting-for-reward component during which mice obtained "free" sucrose pellets with the stipulation that these "free" pellets were delivered at increasing delay intervals.

Results: Coupled with increased FR response rates, mice exposed to postnatal CAPS displayed increased FR resets that reinstated short delays, indicating a preference for shorter delays, despite the added response cost of the FR25. No associated changes in locomotor activity were observed.

Conclusions: Postnatal CAPS exposure produces an enhanced bias towards immediate rewards, a risk factor for several central nervous system (CNS) disorders. This enhancement does not appear to be the result of hyperactivity. The findings underscore the need for further evaluation of air pollution effects on the CNS and its potential contribution to CNS diseases and disorders.

Figure 1

Exposure conditions for animals exposed to CAPS during the early postnatal, young adult, or both exposure periods. Changes in mean particle count (A; left y-axis) closely paralleled changes in mean particle mass concentration (A; right, y-axis). Particles remained < 100 nm (ultrafine) during all exposures (B). Data are reported as group means ± SDs.

Figure 2

FR overall response rates (A), run rates (B), PRP (C), IRT (D), and FR completion time (E) in relation to wait interval during the FR waiting-for-reward schedule for mice exposed to CAPS or filtered air in postnatal, adult, or both exposure periods as indicated. Data are reported as group means ± SEs, of one session each for 5.0 and 12.5 sec, and the mean of two sessions of 7.5 and 10.0 sec and three sessions at 15.0 sec; n = 7–8/treatment group. *p < 0.05 compared with Air/Air animals; **p < 0.05 compared with Air/CAPS-treated animals; p < 0.05 compared with CAPS/Air-treated animals.

Figure 3

FR resets (A), responses per reinforcer (B), long wait time (C), mean wait time (D), and mean wait time/FR completion time (E) for mice exposed to CAPS or filtered air in postnatal, adult, or both exposure periods acquired during FR waiting-for-reward sessions, as indicated. Data are reported as group means ± SEs, of one session each for 5.0 and 12.5 sec, and the mean of two sessions of 7.5 and 10.0 sec and three sessions at 15.0 sec; n = 7–8/treatment group. *p < 0.05 compared with Air/Air animals; **p < 0.05 compared with Air/CAPS-treated animals.

Figure 4

Cumulative records of responding for animals exposed to CAPS or filtered air in postnatal, adult, or both exposure periods while last 15-sec “wait” latency was in effect. The response counter automatically reset to baseline (0 responses) after each 30 responses occurs. As labeled, pips (backslashes) indicate reinforcer delivery, horizontal lines indicate periods of waiting, and vertical lines show FR responding (n = 7–8/treatment group).