Light enhances learned fear

Abstract

The ability to learn, remember, and respond to emotional events is a powerful survival strategy. However, dysregulated behavioral and physiological responses to these memories are maladaptive. To fully understand learned fear and the pathologies that arise during response malfunction we must reveal the environmental variables that influence learned fear responses. Light, a ubiquitous environmental feature, modulates cognition and anxiety. We hypothesized that light modulates responses to learned fear. Using tone-cued fear conditioning, we found that light enhances behavioral responses to learned fear in C57BL/6J mice. Mice in light freeze more in response to a conditioned cue than mice in darkness. The absence of significant freezing during a 2-wk habituation period and during intertrial intervals indicated that light specifically modulates freezing to the learned acoustic cue rather than the context of the experimental chamber. Repeating our assay in two photoreceptor mutant models, Pde6b rd1/rd1 and Opn4 −/− mice, revealed that lightdependent enhancement of conditioned fear is driven primarily by the rods and/or cones. By repeating our protocol with an altered lighting regimen, we found that lighting conditions acutely modulate responses when altered between conditioning and testing. This is manifested either as an enhancement of freezing when light is added during testing or as a depression of freezing when light is removed during testing. Acute enhancement, but not depression, requires both rod/cone-and melanopsin-dependent photoreception. Our results demonstrate a modulation by light of behavioral responses to learned fear.L ight is a pervasive feature of the environment and exerts broad effects on behavior and physiology via two parallel pathways (1). The familiar image-forming visual pathway allows discernment of objects in the environment according to physical qualities: their color, form, texture, and motion. The parallel non-image forming (NIF) pathway enables light to exert numerous effects on physiology and behavior independently of image formation, such as pupil constriction, modulation of heart rate, and the synchronization of circadian rhythms and sleepwake cycles to the daily light-dark cycle (2). In addition to the effects of light on basic physiological functions, light also modulates higher-order cognitive processes, including anxiety, mood, and alertness/awakeness (3, 4). The retina, the sole photosensory organ in mammals, projects directly to brain regions involved in emotional responses. Among these are the amygdala, the bed nucleus of the stria terminalis, and the periaqueductal gray (5). Activity in some of these regions is known to be acutely modulated by light in a wavelength-dependent manner (3, 6), whereas the link between photoreception and function in other retinorecipient emotional processing areas remains to be elucidated.Brain sites involved in emotional processing participate in the critical function of learning and remembering emotionally arousing events. This function enables ...

Modulation of recognition memory performance by light requires both melanopsin and classical photoreceptors

“…Acute light exposure produces a dose-dependent elevation in different measures of arousal in mice, such as corticosterone [50], heart rate and locomotor activity [51], and also enhances conditioned fear responses [13]. However, we do not know how light would affect performance in the object recognition task: would it facilitate or disrupt performance?…”

“…Although the modulatory effects of light on brain network activity in humans are well demonstrated [5–8], the effects of light on cognitive performance are less clear, with varying results across different behavioural tasks [9–11,13–15,34]. Importantly, the retinal photoreceptors that mediate these responses have remained poorly defined.…”

“…These findings complicate interpretation of the role of the melanopsin in regulating memory performance. Moreover, it is unclear if acute light exposure would exert a similar facilitative effect in non-aversive memory tasks, as findings from previous studies suggest that the direction of the effect of light on behavioural performance may vary in different tasks [13–15]. …”

Light as a central modulator of circadian rhythms, sleep and affect

“…In rodents, light has been suggested to enhance the responses to subsequent stimulations in a cued fear conditioning protocol. This response was present if light was only administered at recall (that is, after learning) and was dependent on the presence of rods and cones 129 . Since rods and cones can signal light information through both ipRGCs and conventional RGCs, whether ipRGCs or conventional RGCs are responsible for conveying this information to the brain remained unknown.…”

Blurring the Boundaries of Vision: Novel Functions of Intrinsically Photosensitive Retinal Ganglion Cells

“…Avoidance of light in a light/dark box is melanopsin-108,109 and ipRGC-dependent98 however anxiety from novel environments increases the level of light aversion,98,110 indicating that ipRGCs mediate both innate and anxiety-induced light aversion. The aversive capacity of light is also observed in mice in pavlovian, associative conditioning to a noxious stimulus 111,112. Normal and melanopsin-deficient mice showed enhanced learning in pavlovian fear conditioning, while mice lacking rod and cone photoreceptors did not.…”