Afferent and efferent connections of the diencephalic prepacemaker nucleus in the weakly electric fish,Eigenmannia virescens: interactions between the electromotor system and the neuroendocrine axis

Abstract

The afferent and efferent connections of the gymnotiform central posterior nucleus of the dorsal thalamus and prepacemaker nucleus (CP/PPn) were examined by retrograde and anterograde transport of the small molecular weight tracer, Neurobiotin. The CP/PPn was identified by physiological assay and received a local iontophoretic injection of Neurobiotin. Retrogradely labeled somata were observed in the ventral telencephalon, hypothalamus, and the pretectal nucleus electrosensorius. Anterogradely labeled fibers were traced from the CP/PPn to the ventral telencephalon, the hypothalamus, the neuropil immediately adjacent to the most rostral subdivision of the nucleus electrosensorius, the optic tectum, and the pacemaker nucleus. Retrograde transport of tracer following injections into the ventral telencephalon, preoptic area, lateral hypothalamus, tectum, and pacemaker nucleus confirmed these efferent targets. A rostromedial subarea of the CP/PPn can be identified that projects to basal forebrain regions and to a lateral region of the CP/PPn that contains afferents to the pacemaker. Many of the targets, which are connected with the CP/PPn, have been linked to reproductive behavior or neuroendocrine control in other fishes. A comparative analysis reveals that the efferent pathways of the CP/PPn appear similar and may be homologous to efferent pathways of some components of the auditory thalamus among tetrapods.

Enhanced sensory sampling precedes self-initiated locomotion in an electric fish

“…The Journal of Experimental Biology (2014) include telencephalic regions (Braithwaite, 2005) that are likely homologous with the mammalian pallium and basal ganglia (Wong, 1997;Harvey-Girard et al, 2012;Harvey-Girard et al, 2013). A recent paper (Pereira et al, 2014) has demonstrated that when the telencephalon of Gymnotus omarum is ablated the fish remains quiescent and does not initiate movement for the duration of lengthy experiments.…”

“…Pulse-type electro-sensation thus offers a distinct experimental advantage because each sampling event can be readily and non-invasively monitored from an unrestrained animal (Jun et al, 2012;Jun et al, 2014). In gymnotiform species, EOD pulses are directly driven by a hindbrain pacemaker that is modulated by diencephalic and medullary prepacemaker activity (Heiligenberg et al, 1981;Kawasaki et al, 1988;Dye, 1988;Metzner, 1993;Caputi et al, 1993;Zupanc and Maler, 1997;Wong, 1997;Comas and Borde, 2010). Previous studies of the electromotor circuitry (Caputi et al, 1993;Wong, 1997;Giassi et al, 2012), functional stimulation of an electromotor thalamic nucleus (Comas and Borde, 2010) and drug injection in the pallium (Santana et al, 2001) all indicate a strong modulation of the EODR from the forebrain.…”

“…In gymnotiform species, EOD pulses are directly driven by a hindbrain pacemaker that is modulated by diencephalic and medullary prepacemaker activity (Heiligenberg et al, 1981;Kawasaki et al, 1988;Dye, 1988;Metzner, 1993;Caputi et al, 1993;Zupanc and Maler, 1997;Wong, 1997;Comas and Borde, 2010). Previous studies of the electromotor circuitry (Caputi et al, 1993;Wong, 1997;Giassi et al, 2012), functional stimulation of an electromotor thalamic nucleus (Comas and Borde, 2010) and drug injection in the pallium (Santana et al, 2001) all indicate a strong modulation of the EODR from the forebrain. Thus, the net activity of the higher level neural populations projecting to the EOD pacemaker can be inferred from the time derivative of EODR, or EOD acceleration (EODA) (Metzner, 1993;Metzner, 1999;Arnegard and Carlson, 2005;Pluta and Kawasaki, 2008).…”

Long-term Behavioral Tracking of Freely Swimming Weakly Electric Fish

“…In general, pulse-type species exhibit more variable EOD rate compared to the wave-type species; and animals' EOD rates closely reflect novelty contents of their sensory surroundings 17,18 . Temporal modulations in the EOD rate can reveal higher-level neural activities, since the medullary pacemaker receives direct neural inputs from higher brain regions such as the diencephalic prepacemaker nucleus, which in turn receives axonal projections from the forebrain 19 . However, the EOD timing must be carefully extracted from a raw waveform recording and not biased by the animal's movement-induced distortions.…”

Nonstationary Stochastic Dynamics Underlie Spontaneous Transitions between Active and Inactive Behavioral States

“…Over this period, the EODR creates a complex, bimodal time series that correlates strongly with the movement variable (Fig. 1) and that carries information on neural activity descending from the higher brain centers (Wong, 1997; Giassi et al, 2012a). An adequate model for the EODR would thus give us the ability to characterize, on a phenomenological level, the neural control process underlying spontaneous movement initiation and termination in naturally behaving fish.…”