Maze Learning and Recall in a Weakly Electric Fish, <i>Mormyrus rume proboscirostris</i> Boulenger (Mormyridae, Teleostei)<sup>1</sup>

Walton, Alice G.; Möller, Peter

doi:10.1111/j.1439-0310.2010.01807.x

Cited by 15 publications

(6 citation statements)

References 71 publications

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“…The resulting changes in the transcutaneous electric field are transduced by cutaneous electroreceptors and encoded as train of spikes in primary electroreceptive afferents (Bullock et al, 1961;Fessard and Szabo, 1961;Lissmann, 1958;Szabo and Fessard, 1974;Wright, 1958). This information is further processed in the brain stem (Aumentado-Armstrong et al, 2015;Bell and Maler, 2005;Heiligenberg and Rose, 1985;Kawasaki, 2005) and telencephalon (Harvey Girard et al, 2010;Trinh et al, 2016), giving origin to reflex Post and von der Emde, 1999), stereotyped (Heiligenberg, 1991;Kawasaki, 2005;Moller, 1995) and learned behaviors (Jun et al, 2014;Schumacher et al, 2016;Walton and Moller, 2010).…”

Section: Introductionmentioning

confidence: 99%

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Rodríguez-Cattáneo

Aguilera

Caputi

2017

Journal of Experimental Biology

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As in most sensory systems, electrosensory images in weakly electric fish are encoded in two parallel pathways, fast and slow. From work on wave-type electric fish, these fast and slow pathways are thought to encode the time and amplitude of electrosensory signals, respectively. The present study focuses on the primary afferents giving origin to the slow path of the pulse-type weakly electric fish Gymnotus omarorum. We found that burst duration coders respond with a high-frequency train of spikes to each electric organ discharge. They also show high sensitivity to phase-frequency distortions of the self-generated local electric field. We explored this sensitivity by manipulating the longitudinal impedance of a probe cylinder to modulate the stimulus waveform, while extracellularly recording isolated primary afferents. Resistive loads only affect the amplitude of the re-afferent signals without distorting the waveform. Capacitive loads cause large waveform distortions aside from amplitude changes. Stepping from a resistive to a capacitive load in such a way that the stimulus waveform was distorted, without changing its total energy, caused strong changes in latency, inter-spike interval and number of spikes of primary afferent responses. These burst parameters are well correlated suggesting that they may contribute synergistically in driving downstream neurons. This correlation also suggests that each receptor encodes a single parameter in the stimulus waveform. The finding of waveform distortion sensitivity is relevant because it may contribute to: (a) enhance electroreceptive range in the peripheral 'electrosensory field', (b) a better identification of living prey at the 'foveal electrosensory field' and (c) detect the presence and orientation of conspecifics. Our results also suggest a revision of the classical view of amplitude and time encoding by fast and slow pathways in pulse-type electric fish.

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Section: Introductionmentioning

confidence: 99%

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Rodríguez-Cattáneo

Aguilera

Caputi

2017

Journal of Experimental Biology

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“…Visual guidance during following behavior was excluded by performing all experiments under infrared illumination only, which is invisible to the fish (Ciali et al, 1997). Under these non-visual conditions, the fish could, in principle, use either active electrolocation or the mechanosensory lateral line system (Walton and Moller, 2010) to follow a moving object. In the present study, lateral line stimuli were ruled out by moving the playback dipole inside an electrically transparent agarose tube.…”

Section: Discussionmentioning

confidence: 99%

“…Object-induced local modulations of EOD amplitude and waveform, which are registered by mormyromasts, constitute an electric image that allows the fish to detect and differentiate objects based on their size and shape (von der Emde et al, 2010), as well as material composition (von der Emde, 2006). Active electrolocation is thus used for finding food (von der Emde, 1994;von der Emde and Bleckmann, 1998;Arnegard and Carlson, 2005) and for orientation and navigation in the environment (Cain et al, 1994;Cain and Malwal, 2002;Walton and Moller, 2010;Schumacher et al, 2017b).…”

Section: Introductionmentioning

confidence: 99%

Disembodying the invisible: electrocommunication and social interactions by passive reception of a moving playback signal

Worm

Kirschbaum

Emde

2018

Journal of Experimental Biology

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Mormyrid weakly electric fish have a special electrosensory modality that allows them to actively sense their environment and to communicate with conspecifics by emitting sequences of electric signals. Electroreception is mediated by different types of dermal electroreceptor organs for active electrolocation and electrocommunication, respectively. During electrocommunication, mormyrids exhibit stereotyped discharge sequences and locomotor patterns, which can be induced by playback of electric signals. This raises the question: what sensory information is required to initiate and sustain social interactions, and which electrosensory pathway mediates such interactions? By experimentally excluding stimuli from vision and the lateral line system, we show that can rely exclusively on its electrosensory system to track a mobile source of electric communication signals. Detection of electric playback signals induced discharge cessations, followed by double-pulse patterns. The animals tried to interact with the moving signal source and synchronized their discharge activity to the playback. These behaviors were absent in control trials without playback. Silencing the electric organ in some fish did not impair their ability to track the signal source. Silenced fish followed on trajectories similar to those obtained from intact animals, indicating that active electrolocation is no precondition for close-range interactions based on electrocommunication. However, some silenced animals changed their strategy when searching for the stationary playback source, which indicates passive sensing. Social interactions among mormyrids can therefore be induced and mediated by passive reception of electric communication signals without the need for perception of the location of the signal source through other senses.

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“…In addition, African Mormyrids forage over a long distances but return to a home location over several nights and fish combine active electrosense, sight, and lateral line synergistically in maze acquisition and recall. In the presence of an electric roadmap consisting of an array of metal and plastic objects, fish were able to follow the landmak series [165]. Although, there is still no clear evidence on the mechanisms allowing the fish a long-range allo-centric navigation, it has been suggested that gymnotiformes can use active electroreception for recognizing landmarks and integrate them at the pallium [87,164].…”

Section: Cognitive Abilities Of Weakly Electric Fishmentioning

confidence: 99%

The bioinspiring potential of weakly electric fish

Caputi

2017

Bioinspir. Biomim.

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Electric fish are privileged animals for bio-inspiring man-built autonomous systems since they have a multimodal sense that allows underwater navigation, object classification and intraspecific communication. Although there are taxon dependent variations adapted to different environments, this multimodal system can be schematically described as having four main components: active electroreception, passive electroreception, lateral line sense and, proprioception. Amongst these sensory modalities, proprioception and electroreception show 'active' systems that extrct information carried by self generated forms of energy. This ensemble of four sensory modalities is present in African mormyriformes and American gymnotiformes. The convergent evolution of similar imaging, peripheral encoding, and central processing mechanisms suggests that these mechanisms may be the most suitable for dealing with electric images in the context of the other and self generated actions. This review deals with the way in which biological organisms address three of the problems that are faced when designing a bioinspired electroreceptive agent: (a) body shape, material and mobility, (b) peripheral encoding of electric images, and (c) early processing of electrosensory signals. Taking into account biological solutions I propose that the new generation of underwater agents should have electroreceptive arms, use complex peripheral sensors for encoding the images and cerebellum like architecture for image feature extraction and implementing sensory-motor transformations.

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Maze Learning and Recall in a Weakly Electric Fish, Mormyrus rume proboscirostris Boulenger (Mormyridae, Teleostei)¹

Cited by 15 publications

References 71 publications

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Disembodying the invisible: electrocommunication and social interactions by passive reception of a moving playback signal

The bioinspiring potential of weakly electric fish

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Maze Learning and Recall in a Weakly Electric Fish, Mormyrus rume proboscirostris Boulenger (Mormyridae, Teleostei)1

Cited by 15 publications

References 71 publications

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Disembodying the invisible: electrocommunication and social interactions by passive reception of a moving playback signal

The bioinspiring potential of weakly electric fish

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Product

Resources

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Maze Learning and Recall in a Weakly Electric Fish, Mormyrus rume proboscirostris Boulenger (Mormyridae, Teleostei)¹