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Paul Gamlin; Primate pupillary responses mediated by a novel photopigment. Journal of Vision 2004;4(11):20. doi: 10.1167/4.11.20.
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© ARVO (1962-2015); The Authors (2016-present)
The human pupillary light reflex is one of the most familiar and well studied circuits that link human vision directly to motor behavior, yet its neural control remains mysterious. The pupil reflex is driven by pathways that originate in rod and cone photoreceptors. However, given the rapid desensitization in cone pathways, the sustained constriction of the pupil under photopic conditions is paradoxical. Furthermore, at light OFF, the pupil response often exhibits a brief dilation followed by a paradoxical, sustained pupilloconstriction. Recently a population of intrinsically-photoreceptive retinal ganglion cells has been discovered in rodents that can drive the pupillary light reflex. Since a comparable group of distinctive giant retinal ganglion cells is present in macaque monkey, we sought to determine their influence on primate pupillary responses.
In two rhesus monkeys, we recorded pupillary responses evoked by 10 sec pulses of light at 10 wavelengths between 430 nm and 610 nm over a 6 log unit range. Such responses were recorded under normal conditions and during pharmacological blockade of ON and OFF retinal channels by intravitreal injections of L-AP4 and CNQX. To confirm injection efficacy, the flash electroretinogram was assessed using an Espion system (Diagnosys) equipped with a ColorBurst hand-held mini-Ganzfeld simulator. Following intravitreal injection of L-AP4/CNQX, the b-wave of the ERG was effectively eliminated. Nevertheless, monochromatic illumination between 430 nm and 530 nm elicited both light-evoked pupillary responses and sustained pupilloconstriction following light extinction. The spectral responsivity data for both these responses were well fit by a Vitamin A1 pigment nomogram with a _max of 482 nm. Also, under normal conditions, the spectral responsivity data for the paradoxical, pupilloconstriction were well fit by the same nomogram. Overall, the characteristics of these pupillary responses match the reported spectral sensitivity and kinetics of the intrinsic light response of giant retinal ganglion cells in vitro (Dacey et al., ARVO 2003; Smith et al., ARVO 2003).
In summary, under most photopic conditions, light-evoked pupillary responses reflect a significant contribution from both cones and intrinsic photoreceptive mechanisms. Paradoxical, sustained pupilloconstriction following light extinction reflects a dominant contribution from the intrinsic photoreceptive system. We conclude that all aspects of paradoxical pupil behavior result from the unique response characteristics of the novel photopigment expressed by intrinsically-photoreceptive retinal ganglion cells.
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