This remarkable fish has no cortex but intelligently switches between electrical and vision senses

Is the cortex overrated?
June 27, 2016

The elephantnose fish (Gnathonemus petersii) explores objects in its surroundings by using its eyes or its electrical sense (credit: Timo Moritz)

With its tiny brain (and no cortex), the elephantnose fish (Gnathonemus petersii)* achieves performance comparable to that of humans or other mammals in certain tasks, according to zoologists at the University of Bonn and a colleague from Oxford.

To perceive objects in the water, the fish uses electrolocation (similar to the echolocation of bats) to perceive objects in the water, aided by an electrical organ in its tail, which emits electrical impulses, and numerous electrical sensor organs in its skin. It also uses its visual sense.

Curiously, in an experiment** in which the animals became familiar with an object in an aquarium with the visual sense, they were also able to recognize it again using the electrical sense, although they had never perceived it electrically before.

Experimental setup. Aquarium tanks were divided into two compartments by a partition with two closable gates, behind which were positioned two objects (indicated in red) 1 cm from the gate. Distance grids, which were placed directly behind the gates and which could be passed by pushing them aside, made sure that the fish kept the correct minimal distance to the objects. The larger compartment (experimental area) was again divided into two compartments, one gate leading to each compartment. (credit: S. Schumacher et al./PNAS)

In the experiment, when the two senses delivered different information in the close range of up to two centimeters, the fish trusted only the electrical information and were then “blind” to the visual stimuli. In contrast, for more distant objects, the animals relied above all on their eyes. And they perceived the environment best by using their visual and electrical senses in combination.

“This ability has only been found in mammals, suggesting such a high-level function might be associated with complex mammalian brain structures. Furthermore, the modality-specific inputs are weighted dynamically according to their reliability at different ranges,” the researchers note in a paper published online on PNAS.

“A transfer between the different senses was previously known only for certain highly developed mammals, such as monkeys, dolphins, rats, and humans”, says Professor Gerhard von der Emde at the Institute of Zoology at the University of Bonn. “In a dark, unfamiliar apartment, people feel their way forward to avoid stumbling. When the light goes on, the obstacles felt are recognized by the eye without any problem.”

The secret is in the cerebellum

Parasagittal cresyl violet stained section through the brain of a Gnathonemus petersii showing the topography of the valvulla cerebelli covering most of the rest of the brain.
“Brain” on this figure includes, from left to right, parts of the telencephalon, diencephalon and mesencephalon. (credit: E. Gilissen, based on the material of Prof. J.M. Allman, Caltech)

So exactly how does Gnathonemus petersii achieve this surprising level of intelligence? A clue is provided by Emmanuel Gilissen on the website of The Royal Museum for Central Africa. He explains that the African mormyrids or elephant-nose fishes were noted for having unusually large brains already more than a century ago. “For a mean body mass of 26 g, the mean brain weight of Gnathonemus petersii reaches 0.53 g, almost three times its expected mean value of 0.19 g, as calculated from the relationship between brain size and body size in teleost fish (Kaufman, 2003).

“This character is probably, at least in part, related to their ability to sense prey and to communicate by generating and perceiving electric fields (Nieuwenhuys and Nicholson, 1969).  In contrast with mammals, it is the cerebellum, and not the telencephalon that is greatly enlarged in these fishes. … In elephant-nose fishes, the valvula cerebelli covers most of the rest of the brain.  In contrast, in another highly derived brain such as the human brain, it is the telencephalon, and more specifically the neocortex, a telencephalic structure unique to mammals, that entirely covers the rest of the brain. …

“In the electric fish Gnathonemus petersii, the brain is responsible for approximately 60% of body O2 consumption, a figure three times higher than that for any other vertebrate studied so far, including human.”

So are these electrically genius fish up there with the macaw?

Gnathonemus petersii is widespread in the flowing waters of West Africa and hunts insect larva at dawn and dusk.

** The elephantnose fish was in an aquarium connected to two different chambers; the animal could choose. Behind openings to the chambers there were differently shaped objects: a sphere or a cuboid. The fish learned to steer toward one of these objects by being rewarded with insect larvae. Subsequently, it searched for this object again, to obtain the reward again. When does the fish use a particular sense? To answer this question, the researchers repeated the experiments in absolute darkness. Now the fish could rely only on its electrical sense. As shown by images taken with an infrared camera, it was able to recognize the object only at short distances. With the light on the fish was most successful, because it was able to use its eyes and the electrical sense for the different distances. To find out when the fish used its eyes alone, the researchers made the objects invisible to the electrical sense. Now, the sphere and cuboid to be discriminated had the same electrical characteristics as the water.

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

Most animals use multiple sensory modalities to obtain information about objects in their environment. There is a clear adaptive advantage to being able to recognize objects cross-modally and spontaneously (without prior training with the sense being tested) as this increases the flexibility of a multisensory system, allowing an animal to perceive its world more accurately and react to environmental changes more rapidly. So far, spontaneous cross-modal object recognition has only been shown in a few mammalian species, raising the question as to whether such a high-level function may be associated with complex mammalian brain structures, and therefore absent in animals lacking a cerebral cortex. Here we use an object-discrimination paradigm based on operant conditioning to show, for the first time to our knowledge, that a nonmammalian vertebrate, the weakly electric fish Gnathonemus petersii, is capable of performing spontaneous cross-modal object recognition and that the sensory inputs are weighted dynamically during this task. We found that fish trained to discriminate between two objects with either vision or the active electric sense, were subsequently able to accomplish the task using only the untrained sense. Furthermore we show that cross-modal object recognition is influenced by a dynamic weighting of the sensory inputs. The fish weight object-related sensory inputs according to their reliability, to minimize uncertainty and to enable an optimal integration of the senses. Our results show that spontaneous cross-modal object recognition and dynamic weighting of sensory inputs are present in a nonmammalian vertebrate.