Melanopsin-Derived Visual Responses under Light Adapted Conditions in the Mouse dLGN

Abstract

A direct projection from melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) reaches the primary visual thalamus (dorsal lateral geniculate nucleus; dLGN). The significance of this melanopsin input to the visual system is only recently being investigated. One unresolved question is the degree to which neurons in the dLGN could use melanopsin to track dynamic changes in light intensity under light adapted conditions. Here we set out to address this question. We were able to present full field steps visible only to melanopsin by switching between rod-isoluminant ‘yellow’ and ‘blue’ lights in a mouse lacking cone function (Cnga3-/-). In the retina these stimuli elicited melanopsin-like responses from a subset of ganglion cells. When presented to anaesthetised mice, we found that ~25-30% of visually responsive neurones in the contralateral dLGN responded to these melanopsin-isolating steps with small increases in firing rate. Such responses could be elicited even with fairly modest increases in effective irradiance (32% Michelson contrast for melanopsin). These melanopsin-driven responses were apparent at bright backgrounds (corresponding to twilight-daylight conditions), but their threshold irradiance was strongly dependent upon prior light exposure when stimuli were superimposed on a spectrally neutral ramping background light. While both onset and offset latencies were long for melanopsin-derived responses compared to those evoked by rods, there was great variability in these parameters with some cells responding to melanopsin steps in <1 s. These data indicate that a subset of dLGN units can employ melanopsin signals to detect modest changes in irradiance under photopic conditions.

Signalling by melanopsin (OPN4) expressing photosensitive retinal ganglion cells

“…There is, however, some data concerning the potential roles performed by M4-type pRGCs. The nature and properties of light responses recorded from cells within the dLGN have suggested a role for melanopsin in encoding changes in background [18][19][20] and the modulation of visual responses, with melanopsin reportedly driving adaptation of visual responses, modulating visual feature selectivity and facilitating a more reliable encoding of complex visual signals. 22,23 Based on retrograde labelling studies, it would seem that M4-type pRGCs project almost exclusively to the dLGN, 39 and would, therefore, seem to be predominantly tasked with providing input to visual pathways.…”

“…17 More recently it has become clear that melanopsin contributes not only to a range of NIF pathways but also performs multiple roles in image forming visual pathways. Melanopsin provides visual centres with information regarding overall levels of environmental light, and performs roles in irradiance coding and brightness discrimination, [18][19][20] contrast detection, 21 and adaptation of visual responses. 22 Melanopsin also acts as an irradiance detector for the retina, 22,23 providing measures of overall illuminance and facilitating the adaptation of cone photoresponses under bright-light conditions.…”

Melanopsin supports irradiance‐driven changes in maintained activity in the superior colliculus of the mouse

“…A subset of them, however, project to parts of the early image‐forming visual system, such as the dorsal lateral geniculate nucleus (dLGN) and superficial superior colliculus (sSC) (Dacey et al ., ; Hattar et al ., ; Brown et al ., ; Ecker et al ., ). At the level of the dLGN, ipRGCs appear to be involved in encoding irradiance across scotopic to photopic light conditions (Brown et al ., ; Davis et al ., ; Storchi et al ., ) and have a modulatory role in some spatiotemporal visual properties (Allen et al ., ). However, the significance of the projection of ipRGCs to the sSC is less well explored.…”

Human Visual Cortex Responses to Rapid Cone and Melanopsin-Directed Flicker

“…A major projection of the ipRGCs is to brainstem and hypothalamic sites, where they influence pupil response (Lucas et al, 2003;Gamlin et al, 2007;Tsujimura et al, 2010;Spitschan et al, 2014a) and circadian rhythm (Berson et al, 2002). The ipRGCs project as well to the lateral geniculate nucleus (Dacey et al, 2005;Brown et al, 2010;Brown et al, 2012;Allen et al, 2014) and recent studies suggest that humans are able to perceive variation in melanopsin contrast as variation in brightness (Zaidi et al, 2007;Brown et al, 2012).…”

“…1b). Although the responses of the ipRGCs are notably delayed and prolonged (Dacey et al, 2005), these cells are capable of more rapid signaling. As stimulus intensity rises, the ipRGCs manifest initial transient responses that peak between 200 and 2000 ms (Do et al, 2009).…”