Representation of Auditory Signals in the M-Cell: Role of Electrical Synapses

Abstract

To determine the sensory information encoded and the relative contributions of these two transmission modes, M-cell responses to acoustic stimuli in air were recorded intracellularly. Excitatory postsynaptic potentials (EPSPs) evoked by both short 100-to 900-Hz "pips" and longer-lasting amplitude-and frequency-modulated sounds were dominated by fast, repetitive EPSPs superimposed on an underlying slow depolarization. Fast EPSPs 1) have kinetics comparable to presynaptic action potentials, 2) are maximal on the distal lateral dendrite, and 3) are insensitive to GluR antagonists. They presumably are coupling potentials, and power spectral analysis indicated they constitute a high-pass signal that accurately tracks sound frequency and amplitude. The spatial profile of the slow EPSP suggests both proximal and distal dendritic sources, a result supported by predictions of a multicompartmental model and the effects of AMPAR antagonists, which preferentially reduced the proximal component. Thus a second class of afferents generates a portion of the slow EPSP that, with sound stimuli, demonstrate that the dominant mode of transmission at LMCE synapses is electrical. The slow EPSP is a dynamic, low-pass representation of stimulus strength. Accordingly, amplitude and phase information, which are segregated in other systems, are faithfully represented in the M-cell.

Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus)

“…200·Hz sound waves 50 or 200·ms in duration that increased in intensity exponentially from zero were also used to evoke escapes. These 'ramped' sound waves were used to elicit escapes because, as opposed to pips, they remain constant in frequency and they proved ideal for studying the auditory processing properties of the M-cell (Szabo et al, 2006). In addition, predatory strikes by other fish that evoke C-starts sometimes do not appear to be sudden strikes but rather consist of progressively more powerful multiple body-bends (Harper and Blake, 1991).…”

Social Status–Dependent Shift in Neural Circuit Activation Affects Decision Making

“…Here, we focus on two well-studied behaviors: swimming and the Mauthner-mediated startle escape. The functional and anatomical organization of the underlying neural circuits mediating swim and escape have been studied in larval and adult zebrafish and goldfish (Zottoli, 1977;Zottoli et al, 1987;O'Malley et al, 1996;Ali et al, 2000;Eaton et al, 2001;Severi et al, 2014;Thiele et al, 2014;Wang and McLean, 2014).…”

“…1 A, B). A unilateral stimulus elicits a reflexively fast flexion of the body away from the threat (Eaton et al, 1977;Zottoli, 1977;Zottoli et al, 1987;Eaton and Emberley, 1991;Canfield, 2003;Preuss et al, 2006;Szabo et al, 2006;Weiss et al, , 2009.…”

“…The neural circuit underlying swimming behavior is more distributed, but still displays a clear hierarchical organization (Severi et al, 2014;Thiele et al, 2014;Wang and McLean, 2014). Stimulation of the mesencephalic locomotor region (MLR) evokes swimming (Kashin et al, 1974;Cabelguen et al, 2003).…”

Auditory Input to CNS Is Acquired Coincidentally with Development of Inner Ear after Formation of Functional Afferent Pathway in Zebrafish

“…Zebrafish and goldfish use auditory information effectively to escape quickly from sudden stimuli or predators by firing the Mauthner cells (M-cells) in the hindbrain (Zottoli, 1977;Burgess and Granato, 2007;Kohashi and Oda, 2008). In adult goldfish, it has been established morphologically as well as electrophysiologically that the M-cell is directly innervated by the ipsilateral VIIIth nerve afferents (Furshpan, 1964;Nakajima, 1974;Lin and Faber, 1988;Nakayama and Oda, 2004;Szabo et al, 2006Szabo et al, , 2007. In zebrafish, sound-induced postsynaptic potentials have been recorded in the adult M-cell (Hatta and Korn, 1998), and the earliest contact of the VIIIth nerve afferents with the M-cell occurs at 23 h postfertilization (hpf) (Kimmel et al, 1990).…”