Sensorimotor Integration in Weakly Electric fish
Several species of weakly electric fish inhabit parts of Central and South America, as well as Africa. Their unique electrosensory system, coupled with vision and the mechanosensory lateral line, provides them with multisensory integration which enables them to thrive in the often dark and turbid waters of their habitat. In close collaboration with the Fortune Lab, we investigate several aspects of sensorimotor integration in various species of weakly electric fish. Some previous and current research areas are described below.
Sensorimotor Control of Movement
How is information processed by the nervous system to control locomotion? This fundamental question spawns many of the research topics prevalent in current bio-inspired robotics and systems neuroscience research: neural representations of sensory information, multisensory integration, locomotor and sensory biomechanics, control policies for behavior, adaptation and learning, etc.
To address this question, we study the refuge tracking behavior (see photo on left) exhibited by the weakly electric knifefish Eigenmannia virescens. Eigenmannia robustly and naturally swim back and forth to stabilize visual and/or electrosensory images, just as humans smoothly track moving objects with their eyes to stabilize visual images. This collaborative work applies “robotics” approaches (e.g. system identification, systems and control theory, and signal processing) to understand the nervous system.
For instance, to study how signals from these two parallel sensory streams are used in refuge tracking, we constructed a novel augmented reality apparatus that enables the independent manipulation of visual and electrosensory cues to freely swimming fish. We evaluated the linearity of multisensory integration, the change to the relative perceptual weights given to vision and electrosense in relation to sensory salience, and the effect of the magnitude of sensory conflict on sensorimotor gain.
E. E. Sutton, A. Demir, S. A. Stamper and E. S. Fortune and N. J. Cowan. “Dynamic modulation of visual and electrosensory gains for locomotor control”. J R Soc Interface, 13(118):20160057, 2016. [pdf] [Data and Source Code]
E. Roth, K. Zhuang, S. A. Stamper, E. S. Fortune, and N. J. Cowan. “Stimulus predictability mediates a switch in locomotor smooth pursuit performance for Eigenmannia virescens.” J Exp Biol. 214:1170-1180, 2011. [pdf] [Download cover illustration]
D. Biswas, L. A. Arend, S. A. Stamper, B. P. Vágvölgyi, E. S. Fortune, and N. J. Cowan, “Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip,” Curr Biol, vol. 28, iss. 4, 2018. [pdf]
I. Uyanik, S. Sefati, S. A. Stamper, K. Cho, M. M. Ankarali, E. S. Fortune, and N. J. Cowan, “Variability in locomotor dynamics reveals the critical role of feedback in task control,” eLife,
Active Sensing via Movement
We show that weakly electric fish dramatically adjust their locomotor behavior in relation to changes of modality-specific information. We varied sensory information during a refuge tracking task by changing illumination (vision) and conductivity (electroreception). The gain between refuge movement stimuli and fish tracking responses was functionally identical across all sensory conditions. However, there was a significant increase in the tracking error in the dark (no visual cues). This increase was a result of spontaneous whole-body oscillations (0.1 to 1 Hz) produced by the fish.
These movements were costly: in the dark, fish swam over 3 times further when tracking and produced more net positive mechanical work. The magnitudes of these oscillations increased as electrosensory salience was degraded via increases in conductivity. In addition, tail bending (1.5 to 2.35 Hz), which has been reported to enhance electrosensory perception, occurred only during trials in the dark. These data show that both categories of movements—whole-body oscillations and tail bends—actively shape the spatiotemporal dynamics of electrosensory feedback.
S. A. Stamper, E. Roth, N. J. Cowan, and E. S. Fortune. “Active sensing via movement shapes spatiotemporal patterns of sensory feedback”. J Exp Biol, 215:1567-1574, 2012. [pdf]
I. Uyanik, S. A. Stamper, N. J. Cowan, and E. S. Fortune, “Sensory Cues Modulate Smooth Pursuit and Active Sensing Movements,” Front Behav Neurosci, vol. 13, iss. 59, 2019.
The Jamming Avoidance Response
The Jamming Avoidance Response (JAR) in the weakly electric fish Eigenmannia virescens is an electrosensory behavior whereby the fish’s Electric Organ Discharge (EOD) frequency ‘escapes’ from the frequency of conspecifics. The JAR was discovered in 1961, and has been analyzed at all levels of organization, from whole-organism behavior down to specific ion channels. Nevertheless, a parsimonious description of the JAR behavior in terms of a dynamical system model has not been achieved at least in part due to the fact that “avoidance” behaviors are both intrinsically unstable and nonlinear. An experimental rig by Madhav et. al. overcame the instability of the JAR in Eigenmannia by closing a feedback loop around the behavioral response of the animal. Specifically, the instantaneous frequency of a jamming stimulus was tied to the fish’s own electrogenic frequency by a feedback law. Without feedback, the fish’s own frequency diverges from the stimulus frequency, but appropriate feedback stabilizes the behavior. After stabilizing the system, we measured the responses in the fish’s instantaneous frequency to various stimuli. A delayed first-order linear system model fit the behavior near the equilibrium. Coherence to white noise stimuli together with quantitative agreement across stimulus types supported this local linear model. Next, we examined the intrinsic nonlinearity of the behavior using clamped-frequency-difference experiments to extend the model beyond the neighborhood of the equilibrium. The resulting nonlinear model is composed of competing motor return and sensory escape terms. The model reproduces responses to step and ramp changes in the difference frequency (df) and predicts a “snap-through” bifurcation as a function of df that we confirmed experimentally.
M. S. Madhav, S. A. Stamper, E. S. Fortune, and N. J. Cowan. “Closed-loop stabilization of the jamming avoidance response reveals its locally unstable and globally nonlinear dynamics”. J Exp Biol, 216:4272-4284, 2013. [pdf]
The Social Envelope Response
How is information influenced by the presence of nearby individuals?
To address this question, we examine social behaviors exhibited by the weakly electric knifefish Eigenmannia virescens. Eigenmannia are commonly found in the shallow waters of rivers and streams in the Amazon. Fieldwork has demonstrated that these fish are typically in groups of at least 3 individuals and can be in groups as large as 25 individuals. When fish are in close proximity their electric organ discharges (EODs) mix and produce complex amplitude and phase modulations (AMs and PMs) which are termed a ‘beat’ and second order modulations termed an ‘envelope’.
In a recent study, we investigated the possibility that social context creates envelopes that drive behavior. When Eigenmannia virescens are in groups of three or more, the interactions between their pseudo-sinusoidal electric fields can generate ‘social envelopes’. We developed a simple mathematical prediction for how fish might respond to such social envelopes. To test this prediction, we measured the responses of Eigenmannia to stimuli consisting of two sinusoids, each outside the range of the Jamming Avoidance Response (JAR), that when added to the fish’s own electric field produced low-frequency (below 10 Hz) social envelopes. Fish changed their electric organ discharge (EOD) frequency in response to these envelopes, which we have termed the ‘Social Envelope Response’ (SER). In 99% of trials, the direction of the SER was consistent with the mathematical prediction. The SER was strongest to the lowest initial envelope frequency tested (2 Hz) and depended on stimulus amplitude. The SER generally resulted in an increase of the envelope frequency during the course of a trial, suggesting that this behavior may be a mechanism for avoiding low frequency social envelopes. Importantly, the direction of the SER was not predicted by the superposition of two JAR responses: the SER was insensitive to the amplitude ratio between the sinusoids used to generate the envelope, but was instead predicted by the sign of the difference of difference frequencies (ddF).
S. A. Stamper*, M. S. Madhav*, N. J. Cowan, and E. S. Fortune. “Beyond the Jamming Avoidance Response: Weakly electric fish respond to the envelope of social electrosensory signals”. J Exp Biol, 215:4196-4207, 2012 . [pdf] *Contributed equally. Ranked as one of the top 3 publications in 2012 in J Exp Biol. Highlighted in Inside JEB: “Gregarious Electric Fish Adjust to Maintain Social Envelope”