Electrolocation and electrocommunication in pulse gymnotids: signal carriers, pre-receptor mechanisms and the electrosensory mosaic

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.

Section: Resultsmentioning

confidence: 70%

“…While mormyromasts are complex organs, having two chambers housing two different receptor cell populations innervated by different fibers Szabo, 1974), burst duration coders have a single chamber with a single population of cells innervated by a single fiber (Caputi et al, 2002;Echagüe and Trujillo-Cenóz, 1980;Szabo, 1974).…”

Section: Introductionmentioning

confidence: 99%

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

Rodríguez-Cattáneo

Aguilera

Caputi

2017

“…In Gymnotus carapo, an electric fish lacking a chin appendix, a foveal and parafoveal region at the head of the animals were distinguished Caputi et al, 2002). This contrasts with Gnathonemus petersii where it was proposed (von der Emde and Schwarz, 2002) that the Schnauzenorgan and the nasal region can be considered as two separate electric foveae with different functions: a short-range food classification/detection R. Pusch and others fovea (Schnauzenorgan), and a far-range object detection and guidance system (nasal region) (Castelló et al, 2000;von der Emde, 2006).…”

Section: Discussionmentioning

confidence: 99%

Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation

Pusch

Emde

Hollmann

et al. 2008

SUMMARYWeakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation, nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance, can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response (novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions -the Schnauzenorgan and the nasal region -can be termed electric fovea but they serve separate functions during active electrolocation.

“…Our study deals with Gymnotus omarorum (Richer de Forges et al, 2009), a species in which electrogeneration mechanisms (Macadar, 1993;Caputi, 1999;Caputi et al, 2005), pre-receptor funneling (Caputi and Budelli, 1995;Aguilera et al, 2001), electroreceptor distribution (Castelló et al, 2000;Caputi et al, 2002) and coding (Cilleruelo and Caputi, 2012) are well known.…”

Section: Introductionmentioning

confidence: 99%

The active electrosensory range ofGymnotus omarorum

Pereira

Aguilera

Caputi

2012

Self Cite

SUMMARYThis article reports a biophysical and behavioral assessment of the active electrolocation range of Gymnotus omarorum. Physical measurements show that the stimulus field of a point on the sensory mosaic (i.e. the potential positions in which an object may cause a significant departure of the transcutaneous field from basal in the absence of an object) consists of relatively extended volumes surrounding this point. The shape of this stimulus field is dependent on the position of the point on the receptive mosaic and the size of the object. Although the limit of stimulus fields is difficult to assess (it depends on receptor threshold), departure from the basal field decays rapidly, vanishing at about 1.5 diameters for conductive spheres. This short range was predictable from earlier theoretical constructs and experimental data. Here, we addressed the contribution of three different but synergetic mechanisms by which electrosensory signals attenuate with object distance. Using novelty responses as an indicator of object detection we confirmed that the active electrosensory detection range is very short. Behavioral data also indicate that the ability to precisely locate a small object of edible size decays even more rapidly than the ability to detect it. The role of active electroreception is discussed in the context of the fishʼs habitat.