Time disparity sensitive behavior and its neural substrates of a pulse-type gymnotiform electric fish, Brachyhypopomus gauderio

Abstract

Roles of the time coding electrosensory system in the novelty responses of a pulse-type gymnotiform electric fish, Brachyhypopomus, were examined behaviorally, physiologically, and anatomically. Brachyhypopomus responded with the novelty responses to small changes (100 μs) in time difference between electrosensory stimulus pulses applied to different parts of the body, as long as these pulses were given within a time period of ~500 μs. Physiological recording revealed neurons in the hindbrain and midbrain that fire action potentials time-locked to stimulus pulses with short latency (500-900 μs). These time-locked neurons, along with other types of neurons, were labeled with intracellular and extracellular marker injection techniques. Light and electron microscopy of the labeled materials revealed neural connectivity within the time coding system. Two types of time-locked neurons, the pear-shaped cells and the large cells converge onto the small cells in a hypertrophied structure, the mesencephalic magnocellular nucleus. The small cells receive a calyx synapse from a large cell at their somata and an input from a pear-shaped cell at the tip of their dendrites via synaptic islands. The small cells project to the torus semicircularis. We hypothesized that the time-locked neural signals conveyed by the pear-shaped cells and the large cells are decoded by the small cells for detection of time shifts occurring across body areas.

Encoding phase spectrum for evaluating “electric qualia”

“…In this readout context, one can postulate that centromedial spherical neurons represent the electric image of objects as a latency pattern, while at the lateral map, instead, spherical cells require synchronized input from multiple afferents from a larger region of the skin and may generate a reference signal that can be used downstream for latency decoding. In fact, all spherical neurons project to the magnocellularis nucleus where a Jeffress-like circuit has been described (pulse fish: Réthelyi and Szabó, 1973b;Sotelo et al, 1975;Matsushita et al, 2013;wave fish: Carr et al, 1981).…”

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).…”

“…Accordingly, there is also some evidence suggesting this variable association of lowand high-threshold K + currents in spherical neurons of wave-type electric fish (Mehaffey et al, 2006). Interestingly, a recent article showed that spherical neurons of Brachyhypopomus gauderio, a slow electric organ discharge (EOD) rate pulse gymnotiform that shows large differences in sociality with G. omarorum (Silva et al, 2007), do not exhibit the low responsiveness window and the long refractory period observed in G. omarorum (Matsushita et al, 2012). In addition, it is likely that the expression of high threshold conductance in spherical neurons of the wave-type fish Apteronotus and Eigenmannia allows them to follow the relatively high frequencies of their EODs.…”

“…The large neurons (from which this nucleus takes its name) show multiple processes contacting the small cells, which, in turn, project onto the torus semicircularis (Sotelo et al, 1975;Matsushita et al, 2012). The magnocellular mesencephalic nucleus was postulated to be a coincident detection circuit (Szabo, 1967;Schlegel, 1973;Matsushita et al, 2012).…”

“…This mechanism is an alternative to those shown by pulse mormyriforms and wave-type electric fish for streaming electrosensory signals. Interestingly, pulse species showing a gregarious behavior also lack the long refractory period of homologous spherical neurons (Matsushita et al, 2012), suggesting differences in the sensory hierarchy of active electrolocation and communication signals between both taxa. One-spike-onset neurons may play several functional roles in sensory systems.…”