Cryptic laminar and columnar organization in the dorsolateral pallium of a weakly electric fish

Abstract

In the weakly electric gymnotiform fish, Apteronotus leptorhynchus, the dorsolateral pallium (DL) receives diencephalic inputs representing electrosensory input utilized for communication and navigation. Cell counts reveal that, similar to thalamocortical projections, many more cells are present in DL than in the diencephalic nucleus that provides it with sensory input. DL is implicated in learning and memory and considered homologous to medial and/or dorsal pallium. The gymnotiform DL has an apparently simple architecture with a random distribution of simple multipolar neurons. We used multiple neurotracer injections in order to study the microcircuitry of DL. Surprisingly, we demonstrated that the intrinsic connectivity of DL is highly organized. It consists of orthogonal laminar and vertical excitatory synaptic connections. The laminar synaptic connections are symmetric sparse, random, and drop off exponentially with distance; they parcellate DL into narrow (60 μm) overlapping cryptic layers. At distances greater than 100 μm, the laminar connections generate a strongly connected directed graph architecture within DL. The vertical connectivity suggests that DL is also organized into cryptic columns; these connections are highly asymmetric, with superficial DL cells preferentially projecting towards deeper cells. Our experimental analyses suggest that the overlapping cryptic columns have a width of 100 μm, in agreement with the minimal distance for strong connectivity. The architecture of DL and the expansive representation of its input, taken together with the strong expression of N-methyl-D-aspartate (NMDA) receptors by its cells, are consistent with theoretical ideas concerning the cortical computations of pattern separation and memory storage via bump attractors.

Cross-modal object recognition and dynamic weighting of sensory inputs in a fish

“…Because fish lack an isocortex, the ability of cross-modal object recognition cannot depend on the existence of these mammalian brain structures per se. However, a recent study has shown a cryptic laminar and columnar organization of the dorsolateral pallium (DL) of a gymnotiform weakly electric fish which, together with other organizational structures, supports the hypothesis that there is a homology between the teleost DL and the mammalian cortex (34). Furthermore the pallium of G. petersii is known to receive inputs from the auditory, the visual, the electrosensory, and the lateral line systems (35), and lesion experiments in goldfish have shown that the teleost telencephalon is involved in spatial learning tasks (36)(37)(38), making it a prime candidate for the location of cross-modal object recognition in G. petersii.…”

Vertebrate brains and evolutionary connectomics: on the origins of the mammalian ‘neocortex’

“…The similarities to the findings of Wang et al [20] are quite remarkable and further support the hypothesis of the antiquity of radial microcircuitry and the shared cell and circuit properties of avian and mammalian brains. Recent studies by Maler and co-workers [22] have revealed the presence of similar radially organized microcircuits, mediating electroreception, in the telencephalon of teleost fish. Further studies of the DVR telencephalic circuitry of non-avian reptiles as well as amphibia are clearly needed.…”

Dynamics of Goldfish Subregional Hippocampal Pallium Activity throughout Spatial Memory Formation

“…In mammals, the primary sensory areas of the neocortex present the highest basal CO activity, whereas the limbic and association areas present only low to moderate basal CO levels [Wallace, 1987;Hevner et al, 1995]. Interestingly, it has recently been reported that the teleost Dld is organized in cryptic layers and columns with highly localized intrinsic connectivity, resembling more the mammalian sensory cortex than the hippocampus [Trinh et al, 2016].…”

“…However, Elliott et al [2017] [Rodríguez et al, 2002;Broglio et al, 2010], do not support this proposal. In fact, the highly localized intrinsic connectivity and the expansive input representation in the Dld described in the studies of Elliott et al [2017] and Trinh et al [2016] are more compatible with a multistage heteroassociative network structure that performs competitive learning and pattern association, as in the sensory neocortex, than with the spatially extensive autoassociative architecture of the hippocampus that enables the formation of relational and episodic memories [Amaral and Lavenex, 2007;Rolls and Treves, 1998;Rolls, 2013].…”