Sarah A. Stamper

Jamming avoidance response of big brown bats in target detection

SUMMARY When searching for prey, big brown bats (Eptesicus fuscus) enhance the range of their sonar by concentrating more energy in the nearly constant-frequency (CF) tail portion of their frequency-modulated (FM) sweeps. We hypothesize that this portion of their signals may be vulnerable to interference from conspecifics using the same frequencies in their own emissions. To determine how bats modify their signals when confronted with an interfering stimulus, we compared the echolocation calls of bats when a CF jamming tone was on and off. The bats performed a two-alternative forced-choice detection task in the laboratory that required the use of echolocation. All three bats shifted the tail-end CF component of their emitted frequency bidirectionally away from the CF jamming stimulus only when the jamming frequency was within 2–3 kHz of the preferred baseline frequency of the bat. The duration of their emissions did not differ between the jamming and no-jamming trials. The jamming avoidance response of bats may serve to avoid masking or interference in a narrow range of frequencies important for target detection.

Feedback Control as a Framework for Understanding Tradeoffs in Biology

Control theory arose from a need to control synthetic systems. From regulating steam engines to tuning radios to devices capable of autonomous movement, it provided a formal mathematical basis for understanding the role of feedback in the stability (or change) of dynamical systems. It provides a framework for understanding any system with regulation via feedback, including biological ones such as regulatory gene networks, cellular metabolic systems, sensorimotor dynamics of moving animals, and even ecological or evolutionary dynamics of organisms and populations. Here, we focus on four case studies of the sensorimotor dynamics of animals, each of which involves the application of principles from control theory to probe stability and feedback in an organisms response to perturbations. We use examples from aquatic (two behaviors performed by electric fish), terrestrial (following of walls by cockroaches), and aerial environments (flight control by moths) to highlight how one can use control theory to understand the way feedback mechanisms interact with the physical dynamics of animals to determine their stability and response to sensory inputs and perturbations. Each case study is cast as a control problem with sensory input, neural processing, and motor dynamics, the output of which feeds back to the sensory inputs. Collectively, the interaction of these systems in a closed loop determines the behavior of the entire system.

Perception and coding of envelopes in weakly electric fishes

Summary Natural sensory stimuli have a rich spatiotemporal structure and can often be characterized as a high frequency signal that is independently modulated at lower frequencies. This lower frequency modulation is known as the envelope. Envelopes are commonly found in a variety of sensory signals, such as contrast modulations of visual stimuli and amplitude modulations of auditory stimuli. While psychophysical studies have shown that envelopes can carry information that is essential for perception, how envelope information is processed in the brain is poorly understood. Here we review the behavioral salience and neural mechanisms for the processing of envelopes in the electrosensory system of wave-type gymnotiform weakly electric fishes. These fish can generate envelope signals through movement, interactions of their electric fields in social groups or communication signals. The envelopes that result from the first two behavioral contexts differ in their frequency content, with movement envelopes typically being of lower frequency. Recent behavioral evidence has shown that weakly electric fish respond in robust and stereotypical ways to social envelopes to increase the envelope frequency. Finally, neurophysiological results show how envelopes are processed by peripheral and central electrosensory neurons. Peripheral electrosensory neurons respond to both stimulus and envelope signals. Neurons in the primary hindbrain recipient of these afferents, the electrosensory lateral line lobe (ELL), exhibit heterogeneities in their responses to stimulus and envelope signals. Complete segregation of stimulus and envelope information is achieved in neurons in the target of ELL efferents, the midbrain torus semicircularis (Ts).

Active sensing via movement shapes spatiotemporal patterns of sensory feedback.

SUMMARY Previous work has shown that animals alter their locomotor behavior to increase sensing volumes. However, an animal’s own movement also determines the spatial and temporal dynamics of sensory feedback. Because each sensory modality has unique spatiotemporal properties, movement has differential and potentially independent effects on each sensory system. Here we show that weakly electric fish dramatically adjust their locomotor behavior in relation to changes of modality-specific information in a task in which increasing sensory volume is irrelevant. 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 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 three 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.

Beyond the Jamming Avoidance Response: weakly electric fish respond to the envelope of social electrosensory signals.

SUMMARY Recent studies have shown that central nervous system neurons in weakly electric fish respond to artificially constructed electrosensory envelopes, but the behavioral relevance of such stimuli is unclear. Here we investigate 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 E. virescens to stimuli consisting of two sinusoids, each outside the range of the Jamming Avoidance Response (JAR), that when added to the fishs 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 in response 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.

Echo features used by human listeners to discriminate among objects that vary in material or wall thickness: implications for echolocating dolphins.

Echolocating dolphins extract object feature information from the acoustic parameters of echoes. To gain insight into which acoustic parameters are important for object discrimination, human listeners were presented with echoes from objects used in two discrimination tasks performed by dolphins: Hollow cylinders with varying wall thicknesses (+/-0.2, 0.3, 0.4, and 0.8 mm), and spheres made of different materials (steel, aluminum, brass, nylon, and glass). The human listeners performed as well or better than the dolphins at the task of discriminating between the standard object and the comparison objects on both the cylinders (humans=97.1%; dolphin=82.3%) and the spheres (humans= 86.6%; dolphin= 88.7%). The human listeners reported using primarily pitch and duration to discriminate among the cylinders, and pitch and timbre to discriminate among the spheres. Dolphins may use some of the same echo features as the humans to discriminate among objects varying in material or structure. Human listening studies can be used to quickly identify salient combinations of echo features that permit object discrimination, which can then be used to generate hypotheses that can be tested using dolphins as subjects.

Stimulus predictability mediates a switch in locomotor smooth pursuit performance for Eigenmannia virescens

SUMMARY The weakly electric glass knifefish, Eigenmannia virescens, will swim forward and backward, using propulsion from an anal ribbon fin, in response to motion of a computer-controlled moving refuge. Fish were recorded performing a refuge-tracking behavior for sinusoidal (predictable) and sum-of-sines (pseudo-random) refuge trajectories. For all trials, we observed high coherence between refuge and fish trajectories, suggesting linearity of the tracking dynamics. But superposition failed: we observed categorical differences in tracking between the predictable single-sine stimuli and the unpredictable sum-of-sines stimuli. This nonlinearity suggests a stimulus-mediated adaptation. At all frequencies tested, fish demonstrated reduced tracking error when tracking single-sine trajectories and this was typically accompanied by a reduction in overall movement. Most notably, fish demonstrated reduced phase lag when tracking single-sine trajectories. These data support the hypothesis that fish generate an internal dynamical model of the stimulus motion, hence improving tracking of predictable trajectories (relative to unpredictable ones) despite similar or reduced motor cost. Similar predictive mechanisms based on the dynamics of stimulus movement have been proposed recently, but almost exclusively for nonlocomotor tasks by humans, such as oculomotor target tracking and posture control. These data suggest that such mechanisms might be common across taxa and behaviors.

Closed-loop stabilization of the jamming avoidance response reveals its locally unstable and globally nonlinear dynamics

SUMMARY The Jamming Avoidance Response, or JAR, in the weakly electric fish 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. We overcame the instability of the JAR in Eigenmannia virescens by closing a feedback loop around the behavioral response of the animal. Specifically, the instantaneous frequency of a jamming stimulus was tied to the fishs own electrogenic frequency by a feedback law. Without feedback, the fishs own frequency diverges from the stimulus frequency, but appropriate feedback stabilizes the behavior. After stabilizing the system, we measured the responses in the fishs instantaneous frequency to various stimuli. A delayed first-order linear system model fitted 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.

Detection of targets colocalized in clutter by big brown bats (Eptesicus fuscus)

Echolocating big brown bats (Eptesicus fuscus) frequently catch insects during aerial pursuits in open spaces, but they also capture prey swarming on vegetation, and from substrates. To evaluate perception of targets on cluttered surfaces, big brown bats were trained in a two-alternative forced-choice task to locate a target, varying in height, that was embedded partway in holes (clutter) cut in a foam surface. The holes were colocalized with the possible positions of the target at distances ranging from 25 to 35 cm. For successful perception of the target, the bat had to detect the echoes contributed by the target in the same time window that contained echoes from the clutter. Performance was assessed in terms of target reflective strength relative to clutter strength in the same time window. The bats detected the target whenever the target strength was greater than 1-2 dB above the clutter.

Neuronal connexin expression in the cochlear nucleus of big brown bats.

We present immunohistochemical data describing the presence and distribution of connexins, structural component of gap junctions, in the cochlear nuclei of adult big brown bats (Eptesicus fuscus). Echolocating big brown bats show microsecond scale echo-delay sensitivity that requires accurate synchronization of neuronal responses to the timing of echoes. Midbrain and auditory cortical neuronal response timing is similar to that observed in other non-echolocating mammals, suggesting that lower auditory processing nuclei may have specialized mechanisms for obtaining the required temporal hyperacuity. Our data shows that connexin 36, a gap junction protein specific to neurons, is most densely expressed in the bats cochlear nuclear complex, the medullary region that receives and processes first-order afferents from the auditory nerve. Cx36 expression is absent in the cochlear nucleus of normal mice, which have high-frequency hearing sensitivity similar to big brown bats. Glial connexins, Cx26 and Cx43, expressed in astrocytes and several inner ear structures, are also found in the bat cochlear nucleus complex, associated with major fiber tracts in and around the cochlear nuclei. The extensive presence of neuronally-associated Cx36 in brainstem auditory structures of adult bats suggests a possible role for gap junctions in mediating echo-delay hyperacuity.