Abstract
Purpose::
The functional role of coupling between rods is enigmatic: it can enhance scotopic vision by alleviating saturation at the rod to rod-bipolar cell synapse, but it can also reduce absolute sensitivity by rendering the synapse less effective at separating photon signals from dark noise. Most of what we know about rod coupling comes from studies of cold-blooded vertebrates. However, we also know that rod circuitry in mammals differs significantly from other species; the rod to rod-bipolar pathway is a mammalian specialization, and mammalian rod networks appear distinctive in their limited extent of coupling, proximal localization of junctional contacts, and in the type of connexin proteins underlying the junction. Here we use guinea pig to study these distinctive mammalian junctions.
Methods::
We measured gap junctional conductance directly via simultaneous whole-cell voltage clamp in pairs of neighboring rods. We also analyzed statistical fluctuations in the amplitudes of responses to repeated dim flashes of light as a measure of signal spread between rods. To gauge the spatial extent of coupling, we injected the gap junction permeable tracer Neurobiotin through our patch pipettes.
Results::
Out of 18 rod pairs, 4 showed negligible junctional conductance. The rest showed conductances ranging from 40-360 pS with a mean of 200 pS. In fluctuation analysis of dim flash responses and in Neurobiotin experiments, guinea pig rods showed significant coupling to at most 10 neighboring rods. The gating of gap junctions between guinea pig rods had greater voltage sensitivity than both known Cx35/36 gap junctions from expression systems, as well as putative Cx35/36 junctions between salamander rods.
Conclusions::
The mammalian rod photoreceptor network shows novel properties relative to previously studied systems. Guinea pig rod junctional conductance is an order of magnitude less than that reported in salamander. Accordingly, the mammalian rod network overall shows a lesser degree of signal spread in dim light and appears more limited in spatial extent. Using these new data, we can build a model of the mammalian rod network to better understand its functional role in scotopic vision.
Keywords: photoreceptors • gap junctions/coupling • electrophysiology: non-clinical