Superior Colliculus Lesions Lead to Disrupted Responses to Light in Diurnal Grass Rats (Arvicanthis niloticus)

Abstract

The circadian system regulates daily rhythms of physiology and behavior. Although extraordinary advances have been made to elucidate the brain mechanisms underlying the circadian system in nocturnal species, less is known in diurnal species. Recent studies have shown that retinorecipient brain areas such as the intergeniculate leaflet (IGL) and olivary pretectal nucleus (OPT) are critical for the display of normal patterns of daily activity in diurnal grass rats ( Arvicanthis niloticus). Specifically, grass rats with IGL and OPT lesions respond to light in similar ways to intact nocturnal animals. Importantly, both the IGL and OPT project to one another in nocturnal species, and there is evidence that these 2 brain regions also project to the superior colliculus (SC). The SC receives direct retinal input, is involved in the triggering of rapid eye movement sleep in nocturnal rats, and is disproportionately large in the diurnal grass rat. The objective of the current study was to use diurnal grass rats to test the hypothesis that the SC is critical for the expression of diurnal behavior and physiology. We performed bilateral electrolytic lesions of the SC in female grass rats to examine behavioral patterns and acute responses to light. Most grass rats with SC lesions expressed significantly reduced activity in the presence of light. Exposing these grass rats to constant darkness reinstated activity levels during the subjective day, suggesting that light masks their ability to display a diurnal activity profile in 12:12 LD. Altogether, our data suggest that the SC is critical for maintaining normal responses to light in female grass rats.

Keep Your Mask On: The Benefits of Masking for Behavior and the Contributions of Aging and Disease on Dysfunctional Masking Pathways

“…(C) Olivary pretectal nucleus (OPT) lesions in Nile grass rats result in negative masking to light, but circadian rhythms are unaffected (figure redrawn from Gall et al, 2017 ). (D) Similar to OPT lesions, lesions of the superior colliculus (SC) in Nile grass rats result in negative masking to light, but circadian rhythms are unaffected (figure redrawn from Gall et al, 2020 ).…”

“…In addition, hypothalamic cells are important for regulating many vital functions of the organism, so if too many neurons are destroyed, death of the organism can result (Gall et al, 2016), further complicating lesion studies. One reason that masking may be able to persist even after significant cell death of the SCN is that there are other retinorecipient brain areas that receive direct light input, including the intergeniculate leaflet (IGL), lateral geniculate nucleus (LGN), olivary pretectal nucleus (OPT), and superior colliculus (SC), which have been shown to be heavily involved in masking to light in nocturnal and diurnal organisms (Morin and Allen, 2005;Gall et al, 2013Gall et al, , 2016Gall et al, , 2017Gall et al, , 2020Shuboni-Mulligan et al, 2019). These neural connections and their involvement in the process of masking are outlined in a later section of this review (see "Neural mechanisms underlying masking").…”

“…In nocturnal organisms, the OPT and SC have been shown to be involved in mediating behavioral responses (e.g., sleep) in response to changes in illumination (Miller et al, 1998(Miller et al, , 1999Zhang et al, 2019). In diurnal organisms, when the OPT and SC are lesioned, masking behavior to light is disrupted, but circadian rhythms are not (see Figures 2C,D; Gall et al, 2017Gall et al, , 2020.…”