Normal behavioral responses to light and darkness and the pupillary light reflex are dependent upon the olivary pretectal nucleus in the diurnal Nile grass rat

Abstract

The olivary pretectal nucleus (OPT) is a midbrain structure that receives reciprocal bilateral retinal projections, is involved in the pupillary light reflex, and connects reciprocally with the intergeniculate leaflet (IGL), a retinorecipient brain region that mediates behavioral responses to light pulses (i.e., masking) in diurnal Nile grass rats. Here, we lesioned the OPT and evaluated behavioral responses in grass rats to various lighting conditions, as well as their anxiety-like responses to light exposure. While control grass rats remained diurnal, grass rats with OPT lesions exhibited a more night-active pattern under 12h:12h light-dark (LD) conditions. However, when placed in constant darkness, OPT lesioned grass rats became more active during their subjective day, suggesting that an exaggerated masking response to light may be responsible for the effect of OPT lesions on locomotor activity in LD. To test this hypothesis, we presented dark and light pulses to controls and grass rats with OPT lesions; controls increased their activity in response to light, whereas those with OPT lesions significantly increased activity in response to darkness. Further, when placed in a 7-hr ultradian LD cycle, animals with OPT lesions were more active during darkness than controls. OPT lesions also abolished the pupillary light reflex, but did not affect anxiety-like behaviors. Finally, in animals with OPT lesions, light did not induce Fos expression in the ventrolateral geniculate nucleus, as it did in controls. Altogether, these results suggest that masking responses to light and darkness are dependent upon nuclei within the subcortical visual shell in grass rats.

Circadian and photic modulation of daily rhythms in diurnal mammals

“…Thus, both an intact OPT and IGL are needed for Nile grass rats to show their species typical masking responses, but only the IGL is necessary for the circadian regulation of diurnal behavior in these animals. OPT lesions also abolished the cFOS response in the ventrolateral geniculate nucleus (VGL) to light pulses (Gall et al., ). The projections from ipRGCs to the VGL are reduced in Nile grass rats (Langel et al., ) compared to those of nocturnal rodents (Hattar et al., ).…”

“…The results of experiments identifying areas of the brain that show patterns of cFOS expression that match species differences in behavior has guided lesion studies focusing on the IGL, VSPZ and OPT of Nile grass rats (Figure ; Gall, Shuboni, Yan, Nunez, & Smale, ; Gall, Smale, Yan, & Nunez, ; Gall et al., ). In these animals, IGL lesions reverse the phase preference of the species; post‐surgically the animals were nocturnal in their display of general activity (Gall et al., ).…”

“…The OPT has reciprocal connections with the IGL (Moore, Weis, & Moga, ) and receives retinal inputs from ipRGCs in both nocturnal rodents (Hattar et al., ) and diurnal Nile grass rats (Langel et al., ). In Nile grass rats, lesions of the OPT also had a profound effect on masking responses (Gall et al., ). Like grass rats with IGL lesions, those with OPT damage showed responses to light and dark pulses that resembled those of nocturnal rodents.…”

“…Thus, from the lesion studies with Nile grass rats, the working model that emerges identifies the OPT as necessary for the display of masking responses to light typical of diurnal species, possibly via connections with the VLG and IGL (Gall et al., ). The IGL in turn is not only necessary for normal diurnal masking responses, but is also involved in the circadian regulation of activity (Gall et al., ).…”

The role of vasopressin in olfactory and visual processing

“…This information is then processed by and transmitted through the lateral geniculate nucleus (LGN) of the thalamus to a series of cortical processing areas, where perception of visual stimuli is refined (Priebe and McGee 2014; Sherman and Koch 1986). Light information received by ipRGCs is transmitted directly to the ventrolateral SCN to facilitate photoentrainment and to the olivary pretectal nucleus (OPN) to mediate the pupillary light reflex (Antle et al 2009; Clarke and Ikeda 1985; Gall et al 2017; Hattar et al 2002; Morin 2013). The retina also projects to the superior colliculus (SC) to coordinate proper eye movements and gaze shifts (Klier et al 2001; Lee et al 1988).…”