Sensory flow shaped by active sensing: sensorimotor strategies in electric fish

Abstract

SummaryGoal-directed behavior in most cases is composed of a sequential order of elementary motor patterns shaped by sensorimotor contingencies. The sensory information acquired thus is structured in both space and time. Here we review the role of motion during the generation of sensory flow focusing on how animals actively shape information by behavioral strategies. We use the well-studied examples of vision in insects and echolocation in bats to describe commonalities of sensory-related behavioral strategies across sensory systems, and evaluate what is currently known about comparable active sensing strategies in electroreception of electric fish. In this sensory system the sensors are dispersed across the animalʼs body and the carrier source emitting energy used for sensing, the electric organ, is moved while the animal moves. Thus ego-motions strongly influence sensory dynamics. We present, for the first time, data of electric flow during natural probing behavior in Gnathonemus petersii (Mormyridae), which provide evidence for this influence. These data reveal a complex interdependency between the physical input to the receptors and the animalʼs movements, posture and objects in its environment. Although research on spatiotemporal dynamics in electrolocation is still in its infancy, the emerging field of dynamical sensory systems analysis in electric fish is a promising approach to the study of the link between movement and acquisition of sensory information.

What are cognitive processes? An example-based approach

“…This can be regarded as a form of active sensing strategy, which is also characterized in recent discussions as the perception-action cycle. A further application of the comparator model understood in this way can be seen in the active sensing of objects by weak electric fish (Hofmann et al 2013): weak electric fish have a kind of a sixth sense whereby they register objects by actively producing weak electric fields: elephantnose fish can be trained to recognize different properties of objects based on electrolocation. These properties include the size, distance, impedance, and shape of an object based solely on electric image properties.…”

“…And this can be easily accounted for with the comparator model, where the efference copy provides the key to the difference. The same principle is used in echolocation in bats, who need to distinguish their emitted waves from those of other bats to orient themselves in the environment (Hofmann et al 2013). The same mechanism is also analyzed in detail in singing crickets, where Poulet and Hedwig (2006) have identified the cellular basis of a basic comparator process that is indispensable in order to distinguish self-generated sensory feedback from external information.…”

Rediscovery and description of Paramormyrops sphekodes (Sauvage, 1879) and a new cryptic Paramormyrops (Mormyridae: Osteoglossiformes) from the Ogooué River of Gabon using morphometrics, DNA sequencing and electrophysiology

“…They sense their own EODs as well as those from other individuals using specialized tuberous electroreceptors distributed over the skin surface (Fessard & Szabo, 1961;Bennett, 1965Bennett, , 1971Bass, 1986). These specialized structures serve in two essential functions: electrolocation of objects (Lissmann & Machin, 1958;von der Emde et al, 2008;Hofmann et al, 2013) and intraspecific electrical communication (Möhres, 1957;Moller, 1970Moller, , 1995Moller & Bauer, 1973;Bell, Myers & Russell, 1974;Kramer, 1974;Hopkins & Bass, 1981;Hopkins, 2009), facilitating activity at night or in murky water.…”

Finding and identifying simple objects underwater with active electrosense

“…The fish actively uses both motion and tail bending when identifying underwater objects (Assad et al, 1999;Stamper et al, 2012;Hofmann et al, 2013). Both motion and tail bending give the fish different perspectives and additional information to identify objects.…”