The role of single spiking spherical neurons in a fast sensory pathway

Abstract

SUMMARY One difficulty in understanding the brain is that of linking the structure of the neurons with their computational roles in neural circuits. In this paper we address this subject in a relative simple system, the fast electrosensory pathway of an electric fish, where sensory images are coded by the relative latency of a volley of single spikes. The main input to this path is a stream of discrete electric images resulting from the modulation of a self-generated carrier by the environment. At the second order cell level, a window of low responsiveness, reducing potential interference from other stimuli, follows activation of the path. In the present study, we further characterize the input–output relationship at the second order neurons by recording field potentials, and ascertain its cellular basis using in vitro whole cell patch recordings. The field potentials from freely behaving, socially interacting fish were obtained from chronically implanted fish restrained in a mesh pen. In addition, at the end of some experiments the fish was curarized and the fast electrosensory path responses to artificial stimuli were further explored. These in vivo approaches showed that larger stimuli cause larger and longer windows of low responsiveness. The simple spherical geometry of the second order cells allowed us to unveil the membrane mechanisms underlying this phenomenon in vitro. These spherical cells respond with a single spike at the onset of current steps of any amplitude and duration, showing inward and outward rectification, and a long refractory period. We postulate that a low-threshold K+ conductance generates the outward rectification. The most parsimonious interpretation of our data indicates that slow deactivation of this conductance causes the long refractory period. These non-linear properties of the membrane explain the single spiking profile of spherical cells and the low-responsiveness window observed in vivo. Since the electric organ discharges are emitted at intervals slightly longer than the duration of the low-responsiveness window,we propose that the described cellular mechanisms allow fish streaming self-generated images.

From the intrinsic properties to the functional role of a neuron phenotype: an example from electric fish during signal trade-off

“…This cell phenotype is characteristic of the fast auditory pathways of higher vertebrates, occurring at different processing stages from the cochlear nuclei to the superior coliculi (Bal and Oertel, 2001;Manis and Marx, 1991;Carr, 1993;Koch and Grothe, 2003). They were also reported at the spinal ganglia (Yan et al, 2007) and dorsal horn of mammals (Prescott and De Koninck, 2002) and in the fast electrosensory pathways of gymnotiforms (Nogueira et al, 2006;Matsushita et al, 2012).…”

“…Four lines of argument support this affirmation (Nogueira et al, 2006;Nogueira and Caputi, 2011): (1) subthreshold pulses of increasing intensities are followed by a reduction of the depolarization caused by a second pulse (Fig.3A); (2) action potentials are followed by an increase in cell membrane conductance (Fig.3B) and an increase of spike threshold (Fig.3C) and (3) a long refractory period of similar time course (Fig.3D); and (4) this long refractory period is reduced under the treatment with low doses of the K + channel blocker 4AP (compare Fig.3D and 3E). …”

“…There is a persistent outward rectification dependent on a low-threshold K + conductance (K + LT ), and an inward rectification mediated by a mixed-cation conductance (I h ) (Wu and Oertel, 1984;Manis and Marx, 1991;Reyes et al, 1994;Brew and Forsythe, 1995;Rathouz and Trussell, 1998;Trussell, 1999;Golding et al, 1999;Oertel et al, 2000;Bal and Oertel, 2000;Soares et al, 2002;Koch and Grothe, 2003;MacLeod et al, 2006;Nogueira et al, 2006;Nogueira and Caputi, 2011).…”

“…Due to the one-spike onset response characteristic of the pulse markers and spherical neurons, the population activity evoked by the self-and allo-generated EODs can be recorded as a compound action potential at the nerve, ELL, lateral lemniscus and mesencephalic magnocellular nucleus (Castelló et al, 1998;Nogueira et al, 2006;Nogueira and Caputi, 2011) either in acute experiments or in chronically implanted freely moving fish. The changes in the self-generated local EOD introduced by the presence of objects modulate the firing latency of the pulse marker and spherical neuron axons.…”

“…The amplitude of the compound potential measured in the lateral lemniscus and in the nucleus magnocellularis is dependent on distance and position between fish (as it is expected by the change in the amplitude of the allo-generated electric image). Interestingly, even when both fish remain in a steady relative position, the stimulus-response relationship depends on the interval between the self-and allo-generated EODs (Fig.4) (Castelló et al, 1998;Nogueira et al, 2006;Nogueira and Caputi, 2011). Within a time window lasting approximately 5-10ms after the self-generated EOD, the axons of spherical neurons recorded in the lateral lemniscus and the neurons of the nucleus magnocellularis do not respond to further peripheral stimuli (Fig.4, frame 1, the artifact of the allogenerated EOD is marked as 'a').…”