Normal and rebound impulse firing in retinal ganglion cells

Abstract

Given that the action potential output of retinal ganglion cells (RGCs) determines the nature of the visual information that is transmitted from the retina, an understanding of their intrinsic impulse firing characteristics is critical for an appreciation of the overall processing of visual information. Recordings from RGCs within an isolated whole-mount retina preparation showed that their normal impulse firing from the resting membrane potential (RMP) was linearly correlated in its frequency with the stimulus intensity. In addition to describing the relationship between the magnitude of the current injection and the resulting impulse frequency (F/I relationship), we have characterized the properties of individual action potentials when they are elicited from the RMP. In contrast, hyperpolarizing below the RMP revealed that RGCs displayed a time dependent anomalous rectification, manifested by the appearance of a depolarizing sag in their voltage response. When an adequate period of hyperpolarization was terminated, a fast phasic period of "rebound excitation" was observed, characterized by a brief phasic burst of impulse activity. When compared to equivalent action potential firing evoked by depolarizing from the RMP, rebound spiking was associated with a lower threshold and shorter latency for impulse activation as well as a prominent, phasic, burst-like doublet, or triplet of impulses. The rebound action potential had a more positive voltage overshoot and displayed a higher peak rate of rise in its upstroke than those correspondingly generated by depolarizing current pulses from the RMP. Blocking sodium spikes with TTX confirmed that the preceding hyperpolarization led to the recruitment and subsequent generation of a transient depolarizing voltage overshoot, which we have termed the net depolarizing overshoot (NDO). We propose that the NDO boosts the generation of sodium spikes by triggering rebound spikes on its upstroke and crest, thus accounting for the observed voltage dependent change in the firing pattern of RGCs.

Activation of group I metabotropic glutamate receptors regulates the excitability of rat retinal ganglion cells by suppressing Kir and I h

“…For the inconsistency, the reason may be threefold. Firstly, rebound excitation was triggered by the termination of a sustained hyperpolarization below the resting membrane potential, which is different from action potentials elicited by depolarization from the resting membrane potential (Mitra and Miller 2007a). Secondly, there is different functional state for I h , Kir and low-voltage activated Ca 2?…”

Improved Izhikevich neurons for spiking neural networks

“…Rebound spiking is a phenomenon in which a hyperpolarizing pulse leads to membrane depolarization. It has been accounted as the mechanism behind a variety of neural phenomena (Miltra and Miller 2007;Person and Perkel 2005;Super and Romeo 2011).…”

Ionic mechanisms underlying tonic and phasic firing behaviors in retinal ganglion cells

“…As 2 widely observed firing behaviors in neuronal systems, tonic and phasic firing activities have been found in neurons from different brain regions. [12][13][14][15][16][17][18][19][20] The functional roles for these 2 behaviors have also been subject to intensive investigations during the past decades. For instance, they possess prominent effects in the encoding of reward and punishment signals, 35,36 modulation of conditioned fear behaviors, 37 occupation of dopamine receptors, 38 mediation of behavioral conditioning, 39 and synaptic plasticity.…”

“…Tonic and phasic activities are two typical firing behaviors observed in many types of neurons, e.g., LGN relay neurons, 12 midbrain dopaminergic neurons, 13 pallidal neurons, 14 locus coeruleus neurons, 15 olfactory receptor neurons, 16 and RGCs. [17][18][19][20] Generally speaking, tonic firing refers to a sustained response, which activates during the course of the stimulus; while phasic firing refers to a transient response with one or few action potentials at the onset of stimulus followed by accommodation. It was reported that tonic and phasic activities observed in guinea pig RGCs could be significantly regulated by the activation of cGMP-gated currents.…”