Daily practice of a sustained attention task (SAT) during the light phase of the light/dark cycle causes a stable, entrained, diurnal behavioral activity pattern (Gritton et al. 2009). Following cessation of SAT practice, animals continue to exhibit a diurnal pattern for 8-10 days. As SAT performance is mediated by increases in cortical cholinergic neurotransmission, this experiment assessed levels of acetylcholine (ACh) release across the light and dark cycle of animals that previously performed the SAT at a fixed time. Circadian behavioral activity was recorded, and prefrontal ACh release was measured, using microdialysis, beginning on the third day following the last SAT session. SAT practice took place in either the light phase [ZT4], the dark phase, [ZT16], or in a constant light condition [LL]. A control group practiced a daily fixed interval [FI-9] schedule of reinforcement at ZT4. A second control group was handled at randomly selected times but was neither water-deprived nor performed a task [NP]. Dialysates were collected for 180 min total, beginning 90 min before the prior onset of task practice and again during the equivalent time period twelve hours later. For all animals, ACh release levels were higher during the dark phase. In SAT-performing animals, ACh levels increased for 45 min at ZT4 and ZT16. In addition, the ZT4 animals’ behavioral activity was robustly increased during this interval. Animals trained at ZT4 reversed back to a nocturnal activity pattern 8-10 days after cessation of SAT practice, coinciding with the loss of the task time-synchronized cholinergic activity. A second series of experiments focused on transient increases in cholinergic activity. These transients mediate the actual cue detection process, they are generated by prefrontal glutamatergic-cholinergic interactions, and these interactions are modulated by tonic cholinergic activity such as task time-synchronized increases. Ongoing experiments test the hypothesis that during the prior practice period, spontaneously generated transients occur at a higher frequency, indicative of an enhanced readiness to utilize external cues. Collectively, these results are consistent with the hypothesis that cognitive activity evokes a profound shift of circadian activity and that internal clocks continue to activate the prefrontal attention system precisely at the time of prior practice. Cognitive performance evokes, and is optimized by, synchronization of circadian activity with the performance period. Cholinergic inputs to the cortex mediate performance and also contribute to circadian shifts, and in turn become subject to circadian control.
Staying cognitively engaged during the wrong time of the day: cognitive-cholinergic induction and maintenance of diurnality in rats
Paolone GConceptualization
;
2010-01-01
Abstract
Daily practice of a sustained attention task (SAT) during the light phase of the light/dark cycle causes a stable, entrained, diurnal behavioral activity pattern (Gritton et al. 2009). Following cessation of SAT practice, animals continue to exhibit a diurnal pattern for 8-10 days. As SAT performance is mediated by increases in cortical cholinergic neurotransmission, this experiment assessed levels of acetylcholine (ACh) release across the light and dark cycle of animals that previously performed the SAT at a fixed time. Circadian behavioral activity was recorded, and prefrontal ACh release was measured, using microdialysis, beginning on the third day following the last SAT session. SAT practice took place in either the light phase [ZT4], the dark phase, [ZT16], or in a constant light condition [LL]. A control group practiced a daily fixed interval [FI-9] schedule of reinforcement at ZT4. A second control group was handled at randomly selected times but was neither water-deprived nor performed a task [NP]. Dialysates were collected for 180 min total, beginning 90 min before the prior onset of task practice and again during the equivalent time period twelve hours later. For all animals, ACh release levels were higher during the dark phase. In SAT-performing animals, ACh levels increased for 45 min at ZT4 and ZT16. In addition, the ZT4 animals’ behavioral activity was robustly increased during this interval. Animals trained at ZT4 reversed back to a nocturnal activity pattern 8-10 days after cessation of SAT practice, coinciding with the loss of the task time-synchronized cholinergic activity. A second series of experiments focused on transient increases in cholinergic activity. These transients mediate the actual cue detection process, they are generated by prefrontal glutamatergic-cholinergic interactions, and these interactions are modulated by tonic cholinergic activity such as task time-synchronized increases. Ongoing experiments test the hypothesis that during the prior practice period, spontaneously generated transients occur at a higher frequency, indicative of an enhanced readiness to utilize external cues. Collectively, these results are consistent with the hypothesis that cognitive activity evokes a profound shift of circadian activity and that internal clocks continue to activate the prefrontal attention system precisely at the time of prior practice. Cognitive performance evokes, and is optimized by, synchronization of circadian activity with the performance period. Cholinergic inputs to the cortex mediate performance and also contribute to circadian shifts, and in turn become subject to circadian control.
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