Species-Specific Diversity of a Fixed Motor Pattern: The Electric Organ Discharge of Gymnotus

Understanding fixed motor pattern diversity across related species provides a window for exploring the evolution of their underlying neural mechanisms. The electric organ discharges of weakly electric fishes offer several advantages as paradigmatic models for investigating how a neural decision is transformed into a spatiotemporal pattern of action. Here, we compared the far fields, the near fields and the electromotive force patterns generated by three species of the pulse generating New World gymnotiform genus Gymnotus. We found a common pattern in electromotive force, with the far field and near field diversity determined by variations in amplitude, duration, and the degree of synchronization of the different components of the electric organ discharges. While the rostral regions of the three species generate similar profiles of electromotive force and local fields, most of the species-specific differences are generated in the main body and tail regions of the fish. This causes that the waveform of the field is highly site dependant in all the studied species. These findings support a hypothesis of the relative separation of the electrolocation and communication carriers. The presence of early head negative waves in the rostral region, a species-dependent early positive wave at the caudal region, and the different relationship between the late negative peak and the main positive peak suggest three points of lability in the evolution of the electrogenic system: a) the variously timed neuronal inputs to different groups of electrocytes; b) the appearance of both rostrally and caudally innervated electrocytes, and c) changes in the responsiveness of the electrocyte membrane

The correlations between the two main peaks indicate different responsiveness of the electrocytes.

<p>The late negative peaks (V₄) recorded in air gap conditions from 6 regions of the body were plotted as a function of the main positive peaks (V₃) recorded from the same 6 regions. It is shown that the relationship between these components is similar in different fish. Different symbols indicate different specimens (<i>G omari</i> N = 10; G. <i>carapo</i> N = 4; <i>G coropinae</i> N = 10). In <i>G. omari</i> V₃ is generally larger than V₄ while in <i>G carapo</i> and <i>G. coropinae</i> they are similar. Since the putative mechanism of V₄ is the propagation of the action potential causing V₃ to the opposite electrocyte face, changes in the slope indicate that the responsiveness of the electrocytes is different for each species-the lowest for <i>G. omari</i>, and the largest for <i>G. coropinae</i>.</p

Head to tail electric organ discharges.

<p>Electric organ discharge waveform (a) and spectral power density (b) for 15 adult specimens of <i>Gymnotus carapo, G. coropinae</i> (both from Surinam), and <i>G. omari</i> (from Uruguay). Electric organ discharges were plotted with head positivity upwards, normalized and aligned to the peak amplitude of the dominant positive peak (P₁). Scale bar = 1 ms. We indicate here the wave components using the two nomenclatures available from the literature. The nomenclature by Trujillo-Cenòz et al. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone.0002038-TrujilloCenz1" target="_blank">[44]</a> is based on the ordinal number of wave components (labeled as V) in the sequence of deflections observed at the head to tail recordings. These components were defined not only by their presence in the head to tail recordings but also by their different origin and mechanisms of generation <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone.0002038-Caputi2" target="_blank">[6]</a>. Crampton's <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone.0002038-Crampton2" target="_blank">[38]</a> nomenclature (used in several species of the genus) refers only to the ordinal number of each peak (P) in the head to tail recordings, referring to P₁ as the main positive peak. For <i>G. omari</i>, P₀ = V₁ + V₂, P₁ = V₃, P₂ = V₄. The application of a wave components based nomenclature to the head to tail recordings of <i>G. carapo</i> and <i>G. coropinae</i> is impossible because head to tail peaks are just the weighted sum of several waveform components of different origin, and probably generation mechanisms, which occur overlapped in time. Instead, we introduce a new nomenclature with a numeral sub index indicating the temporal order and a literal sub index indicating the spatial origin (r for rostral, c for central, and t for tail, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone-0002038-g005" target="_blank">Fig. 5</a> for the pattern of electromotive forces and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone-0002038-g008" target="_blank">Fig. 8</a> summarizing our hypothesis on the electric organ discharge generators)</p

Transcutaneous current pattern of <i>G. carapo</i>.

<p>Electric field perpendicular to the main axis of the fish body was recorded along a line 2 mm parallel to the fish side of <i>G. carapo</i> (same resolution and color code as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone-0002038-g002" target="_blank">Figure 2</a>). This species shows the more complicated generator. We refer to each generator referring to its temporal order (numeral sub index) and spatial origin (literal sub index, r for rostral, c for central, and t for tail). Times are referred to the positive peak (0 ms). The first observed activity is caused by a much localized sink at the head and a source distributed on the abdominal region (reversal point about 10–15% of the fish length from the jaw, V_1r). It is followed by a distributed activity corresponding to more than one generator. In fact, two sinks at the head and at the tail regions indicate two simultaneous spots of activity in the electric organ at about 0.8 ms before the positive peak (reversal points about 20 and 75%,). Half a ms later the rostral activity reverses direction while at the central region a more distributed sink (having its source at the tail) develops. The complex V_34ct (labels: 0 and 0.5 ms) has the same profile as in the other species and finally the electric organ discharge ends with a rebound (label: 1.1 ms, V₅).</p

Transcutaneous current pattern of <i>G. coropinae</i>.

<p>Electric fields perpendicular to the main axis of the fish body was recorded along a line 2 mm parallel to the fish side in <i>G. coropinae</i> (same resolution and color code as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone-0002038-g002" target="_blank">Figure 2</a>). We refer to each generator referring to its temporal order (numeral sub index) and spatial origin (literal sub index, r for rostral, c for central, and t for tail). Times are referred to the positive peak (0 ms). This species is characterized by a first observed activity caused by a much localized sink at the head region (note that the reversal point, rostral sink-caudal source, 1.3 ms before the head to tail peak is located almost about the rostral pole of the fish). After a relative long period of time (−0.2 ms) this wave is followed by two spots activity indicated by the presence of two sources (at the head and at the tail) draining the current that sinks along the central body region. Shortly after the above, the fish's body becomes active. The complex V_34ct (0 to 0.2 ms) has the same profile as in the other species. Finally the electric organ discharge ends with a small rebound wave (0.4 ms, V₅).</p

Transcutaneous current pattern of <i>G. omari</i>.

<p>Electric field perpendicular to the main axis of the fish body was recorded along a line 2 mm parallel to the mid-flank of <i>G. omari</i>. White traces correspond to the recorded field at equally separated points 2 mm from the skin on the side of the fish. These traces are superimposed on a color-map indicating the location of the sources (yellow-red-brown) and sinks (sky blue-deep blue) along the fish body (vertical axis) as the electric organ discharge progresses in time (horizontal axis); greenish correspond to negligible fields. <i>G. omari</i> shows 4 main components: V_1r inverting about the origin of the anal fin; V_2c inverting about half of the body; V_3rct and V_4ct inverting at the tail region. In this case there is a close correlation between temporal order and spatial origin of the components. For the sake of generality we used numeral sub index indicating the temporal order and a literal sub index indicating the spatial origin (r for rostral, c for central, and t for tail).</p

Top row: Comparison between rms values of the head to tail electric organ discharge as measured in the same tank (45×26×4) at the same water conductivity and temperature.

<p>Bottom row: the same individual values were normalized by the square of the fish's length according to the findings of Pereira et al <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0002038#pone.0002038-Pereira1" target="_blank">[18]</a>. Columns: median and interquartile range for each species. All these fish were recorded between 10 to 20 days after capture.</p