Neural activation in arousal and reward areas of the brain in day-active and night-active grass rats

Abstract

In the diurnal unstriped Nile grass rat (Arvicanthis niloticus) access to a running wheel can trigger a shift in active phase preference, with some individuals becoming night-active (NA), while others continue to be day-active (DA). To investigate the contributions of different neural systems to the support of this shift in locomotor activity, we investigated the association between chronotype and Fos expression during the day and night in three major nuclei in the basal forebrain (BF) cholinergic (ACh) arousal system – medial septum (MS), vertical and horizontal diagonal band of Broca (VDB and HDB respectively) –, and whether neural activation in these areas was related to neural activity in the orexinergic system. We also measured Fos expression in dopaminergic and non-dopaminergic cells of two components of the reward system that also participate in arousal – the ventral tegmental area (VTA) and supramammillary nucleus (SUM). NAs and DAs were compared to animals with no wheels. NAs had elevated Fos expression at night in ACh cells, but only in the HDB. In the non-cholinergic cells of the BF of NAs, enhanced nocturnal Fos expression was almost universally seen, but only associated with activation of the orexinergic system for the MS/ VDB region. For some of the areas and cell types of the BF, the patterns of Fos expression of DAs appeared similar to those of NAs, but were never associated with activation of the orexinergic system. Also common to DAs and NAs was a general increase in Fos expression in non-dopaminergic cells of the SUM and anterior VTA. Thus, in this diurnal species, voluntary exercise and a shift to a nocturnal chronotype changes neural activity in arousal and reward areas of the brain known to regulate a broad range of neural functions and behaviors, which may be also affected in human shift workers.

Plastic oscillators and fixed rhythms: Changes in the phase of clock-gene rhythms in the PVN are not reflected in the phase of the melatonin rhythm of grass rats

“…Although species differences may be responsible for these divergent outcomes, these observations nevertheless support the view that voluntary reversals of the phase of activity (present study) affect the brain and the circadian system in a fashion that differs from the effects of forced-activity paradigms (Karatsoreos et al, 2011, McDonald et al, 2013, Saderi et al, 2013, Hsieh et al, 2014). In agreement with this view are the results of direct comparisons of the effects on the brain of spontaneous and forced wakefulness (Castillo-Ruiz et al, 2010, Castillo-Ruiz and Nunez, 2011). Thus, in grass rats, voluntary nocturnal wakefulness results in increased neuronal activation, as indicated by Fos expression, in reward areas of the brain (i.e., horizontal diagonal band, ventral tegmental area, and supramammillary nuclei; Castillo-Ruiz et al,2010), which is an observation not extended to studies using a forced-wakefulness paradigm with the same species (Castillo-Ruiz and Nunez, 2011) The NA grass rat appears to be an attractive model to understand the consequences of activity during the rest phase in a diurnal species, without the effects of the stress associated with forced-wakefulness paradigms (Castillo-Ruiz and Nunez, 2011).…”

Sleep disorders, obesity, and aging: The role of orexin

“…Orexin neurons appear to synapse directly on basal forebrain cholinergic neurons important in cognition (Castillo-Ruiz et al, 2010; Fadel et al, 2005; Frederick-Duus et al, 2007), and orexin appears to mediate long-term potentiation in the dentate gyrus of the hippocampus (Akbari et al, 2011). Prior work utilizing operant tasks shows that supplementing orexin might affect cognitive processes (Choi et al, 2010; Sharf et al, 2010; Thorpe et al, 2005).…”

Day–night differences in neural activation in histaminergic and serotonergic areas with putative projections to the cerebrospinal fluid in a diurnal brain

“…1A). Finally, a 160 μm 2 sampling box was placed in the caudal SUM, as described previously (Castillo-Ruiz et al, 2010). …”

“…The mDR, MR, and SUM did not require this procedure since these regions extended across the midline (see Fig. 1 and Castillo-Ruiz et al, 2010). In addition, for the lDR and all levels of the mDR cell counts were divided by the area occupied by their sampling box and the results are expressed as number of cells/mm 2 .…”