Organization of the gymnotiform fish pallium in relation to learning and memory: III. Intrinsic connections

Abstract

The present article reports on the telencephalic connections of regions of the dorsal telencephalon of the weakly electric fish Apteronotus leptorhynchus and Gymnotus sp. that are involved in learning and memory: the lateral (DL), central (DC), and dorsal (DD) regions of the pallium and the intermediate region between DL and DC (Dx). We find that the main route of transmission consists of diencephalic (preglomerular complex; PG) glutamatergic input to DL; glutamatergic projections from DL to DC and Dx; and glutamatergic output from DC/Dx to di-, mes-, and rhombencephalic nuclei. Although PG efferents to DL are spatially organized, the projection from DL to DC appears to be diffuse. The connections of DD are entirely intrinsic to the pallium: DL projects to DD (glutamatergic) and DD feeds back to DL (glutamatergic); DD also projects to DC and has strong contralateral connections. In addition, DL and DD receive input from subpallial regions; we suggest that these are associated with the previously identified γ-aminobutyric acid (GABA)-ergic, dopaminergic, and somatostatin-positive input to these regions. The DL/DD connections are very complex, because DL projects to and receives input from different subdivisions of DD. These subdivisions are linked by circuitry intrinsic to DD itself. DL and DD both contain recurrent putatively excitatory (glutamatergic) connections as well as local putatively inhibitory (GABAergic) interneurons. In contrast, recurrent excitatory connections appears to be absent in DC, and local inhibition is also barely present. Finally, we speculate on the implications of this pattern of connectivity for theories of short-term memory and long-term associative memory.

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

“…On the basis of previous results (Giassi et al 2012b;HarveyGirard et al 2010), we further propose that Up state activity is an important factor in the consolidation of memories in the DD/DL/DC network. This conclusion is consistent with the importance of DD for trace conditioning in goldfish (Vargas et al 2009).…”

“…DL and DD form a feedback loop, and both structures consist of intrinsic recurrent networks (Giassi et al 2012b), and this complex circuitry presumably underlies the variability of Up state induction and maintenance. Alternatively, it is therefore also possible that the Up states are caused by DD recurrent network activity that is first initiated by DL input, or even by some combination of DL and DD recurrent network activity.…”

“…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.…”

“…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. DD and the pallial regions with which it interconnects (Giassi et al 2012b) may therefore prove to be a useful model system for the study of the long time scale neural processes associated with cognition, learning, and memory formation.…”

“…Instead, DD interconnects various pallial and subpallial regions (Giassi et al 2012b), suggesting that its activity is indicative of cognitive processes. DD and the pallial regions with which it interconnects (Giassi et al 2012b) may therefore prove to be a useful model system for the study of the long time scale neural processes associated with cognition, learning, and memory formation. …”