Organization of the gymnotiform fish pallium in relation to learning and memory: II. Extrinsic connections

Abstract

This study describes the extrinsic connections of the dorsal telencephalon (pallium) of gymnotiform fish. We show that the afferents to the dorsolateral and dorsomedial pallial subdivisions of gymnotiform fish arise from the preglomerular complex. The preglomerular complex receives input from four clearly distinct regions: (1) descending input from the pallium itself (dorsomedial and dorsocentral subdivisions and nucleus taenia); (2) other diencephalic nuclei (centroposterior, glomerular, and anterior tuberal nuclei and nucleus of the posterior tuberculum); (3) mesencephalic sensory structures (optic tectum, dorsal and ventral torus semicircularis); and (4) basal forebrain, preoptic area, and hypothalamic nuclei. Previous studies have implicated the majority of the diencephalic and mesencephalic nuclei in electrosensory, visual, and acousticolateral functions. Here we discuss the implications of preglomerular/pallial electrosensory-associated afferents with respect to a major functional dichotomy of the electric sense. The results allow us to hypothesize that a functional distinction between electrocommunication vs. electrolocation is maintained within the input and output pathways of the gymnotiform pallium. Electrocommunication information is conveyed to the pallium through complex indirect pathways that originate in the nucleus electrosensorius, whereas electrolocation processing follows a conservative pathway inherent to all vertebrates, through the optic tectum. We hypothesize that cells responsive to communication signals do not converge onto the same targets in the preglomerular complex as cells responsive to moving objects. We also hypothesize that efferents from the dorsocentral (DC) telencephalon project to the dorsal torus semicircularis to regulate processing of electrocommunication signals, whereas DC efferents to the tectum modulate sensory control of movement.

Stimulus-induced up states in the dorsal pallium of a weakly electric fish

“…Both results, as well our earlier data on learning-associated induction of Egr-1 expression, indicate that the activity of DD cells is not clearly and immediately linked to sensory input but is modulated by such input over very long time scales. DD is the highest level of the gymnotiform brain in the sense that, unlike other pallial regions, it does not receive direct sensory input from PG or project to brain stem motor regions, e.g., tectum (Giassi et al 2012a(Giassi et al , 2012b. Instead, DD interconnects various pallial and subpallial regions (Giassi et al 2012b), suggesting that its activity is indicative of cognitive processes.…”

“…This led us to hypothesize that DD was involved in detecting novel stimuli and initiating long-term memory storage of the beat frequency in the large dorsolateral pallium (DL). DD receives glutamergic input from DL, which, in turn, receives a sparsely encoded representation of electrosensory features, including AM (beat) stimuli, as well as acoustic input from a thalamic analog, the preglomerular nucleus (PG) (Giassi et al 2012a). DD then projects back to DL via glutamatergic synapses.…”

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

“…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).…”

Enhanced attention precedes self-initiated locomotion in an electric fish

“…The dorsal telencephalon is required for spatial learning in teleosts and might initiate movement via its projections to the tectum [6]. Our results therefore suggest that comparative studies of the neural basis of volition may therefore be possible in pulse-type electric fish, given the substantial homologies between the telencephali of electric fish and mammals.…”