Eric S. Fortune

Short-term synaptic plasticity as a temporal filter

Synaptic efficacy can increase (synaptic facilitation) or decrease (synaptic depression) markedly within milliseconds after the onset of specific temporal patterns of activity. Recent evidence suggests that short-term synaptic depression contributes to low-pass temporal filtering, and can account for a well-known paradox - many low-pass neurons respond vigorously to transients and the onsets of high temporal-frequency stimuli. The use of depression for low-pass filtering, however, is itself a paradox; depression induced by ongoing high-temporal frequency stimuli could preclude desired responses to low-temporal frequency information. This problem can be circumvented, however, by activation of short-term synaptic facilitation that maintains responses to low-temporal frequency information. Such short-term plasticity might also contribute to spatio-temporal processing.

Distributed representation in the song system of oscines: evolutionary implications and functional consequences.

This paper reviews the organizational principles and implications that have emerged from the analysis of HVc, a forebrain nucleus that is a major site of sensory, motor, and sensorimotor integration in the song control system of oscine passerine birds (songbirds). Anatomical, physiological, and behavioral data support the conclusion that HVc exists within a hierarchically organized system with parallel pathways that converge onto HVc. The organization of HVc is distributed and redundant, and its outputs exhibit broad divergence. A similar pattern of connectivity exists for neostriatum adjacent to HVc. This and other data support the hypothesis that the song system arose from an elaboration or duplication of pathways generally present in all birds. Spontaneous and auditory response activity is strongly correlated throughout HVc, with auditory responses exhibiting strong temporal modulation in a synchronized fashion throughout the nucleus. This suggests that the auditory representation of song is encoded in the synchronized temporal patterns of activation, and that the predominant selectivity for the individuals own song that is observed for HVc neurons results from interactions of auditory input with central pattern generators for song. Most, or all HVc neurons are recruited during singing. The auditory response and motor recruitment properties of individual HVc neurons have no simple relationship, and the spontaneous activity in HVc may build up in the seconds preceding a song. To the extent HVc participates in perceptual phenomena associated with song, production and perception are not tightly linked in adults but may be linked by shared developmental processes during periods of sensorimotor learning.

The Critical Role of Locomotion Mechanics in Decoding Sensory Systems

How do neural systems process sensory information to control locomotion? The weakly electric knifefish Eigenmannia, an ideal model for studying sensorimotor control, swims to stabilize the sensory image of a sinusoidally moving refuge. Tracking performance is best at stimulus frequencies less than ∼1 Hz. Kinematic analysis, which is widely used in the study of neural control of movement, predicts commensurately low-pass sensory processing for control. The inclusion of Newtonian mechanics in the analysis of the behavior, however, categorically shifts the prediction: this analysis predicts that sensory processing is high pass. The counterintuitive prediction that a low-pass behavior is controlled by a high-pass neural filter nevertheless matches previously reported but poorly understood high-pass filtering seen in electrosensory afferents and downstream neurons. Furthermore, a model incorporating the high-pass controller matches animal behavior, whereas the model with the low-pass controller does not and is unstable. Because locomotor mechanics are similar in a wide array of animals, these data suggest that such high-pass sensory filters may be a general mechanism used for task-level locomotion control. Furthermore, these data highlight the critical role of mechanical analyses in addition to widely used kinematic analyses in the study of neural control systems.

NEW TECHNIQUES FOR MAKING WHOLE-CELL RECORDINGS FROM CNS NEURONS IN VIVO

Abstract Patch-type pipettes increasingly are being used to obtain intracellular ‘whole-cell’ recording from neurons. Here we describe our methods for making whole-cell recordings in vivo from midbrain neurons in an electric fish. Novel elements in the procedure are: A device for micropositioning the pipette when near a cell use of a ‘Picospritzer’ for cleaning the pipette tip and cell surface, and an electroporetic method, for perforating the patch following seal formation. In addition, we show that extracellular and intracellular recordings can be made from the same neuron. Stable intracellular recordings can be made from neurons at least as small as 10 μm.

Parallel Coding of First- and Second-Order Stimulus Attributes by Midbrain Electrosensory Neurons

Natural stimuli often have time-varying first-order (i.e., mean) and second-order (i.e., variance) attributes that each carry critical information for perception and can vary independently over orders of magnitude. Experiments have shown that sensory systems continuously adapt their responses based on changes in each of these attributes. This adaptation creates ambiguity in the neural code as multiple stimuli may elicit the same neural response. While parallel processing of first- and second-order attributes by separate neural pathways is sufficient to remove this ambiguity, the existence of such pathways and the neural circuits that mediate their emergence have not been uncovered to date. We recorded the responses of midbrain electrosensory neurons in the weakly electric fish Apteronotus leptorhynchus to stimuli with first- and second-order attributes that varied independently in time. We found three distinct groups of midbrain neurons: the first group responded to both first- and second-order attributes, the second group responded selectively to first-order attributes, and the last group responded selectively to second-order attributes. In contrast, all afferent hindbrain neurons responded to both first- and second-order attributes. Using computational analyses, we show how inputs from a heterogeneous population of ON- and OFF-type afferent neurons are combined to give rise to response selectivity to either first- or second-order stimulus attributes in midbrain neurons. Our study thus uncovers, for the first time, generic and widely applicable mechanisms by which parallel processing of first- and second-order stimulus attributes emerges in the brain.

Neural mechanisms for the coordination of duet singing in wrens.

The brains of duetting wrens encode the entire song and not just the contribution of the individual. Plain-tailed wrens (Pheugopedius euophrys) cooperate to produce a duet song in which males and females rapidly alternate singing syllables. We examined how sensory information from each wren is used to coordinate singing between individuals for the production of this cooperative behavior. Previous findings in nonduetting songbird species suggest that premotor circuits should encode each bird’s own contribution to the duet. In contrast, we find that both male and female wrens encode the combined cooperative output of the pair of birds. Further, behavior and neurophysiology show that both sexes coordinate the timing of their singing based on feedback from the partner and suggest that females may lead the duet.

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.

The decoding of electrosensory systems.

Progress in the study of electrosensory systems has been facilitated by the systematic use of behavior as a tool to probe the nervous system. Indeed, a specific behavior that is found in a subset of weakly electric fishes, the jamming avoidance response, was used to identify and characterize an entire suite of brain circuits, from sensory receptors to motor units, that are involved in control of this behavior. Recent progress has focused on a re-analysis of this circuit in relation to newly described electrosensory behaviors, including prey capture, social signaling and the tracking of electrosensory objects. This re-analysis has led to a re-evaluation of the broader functional relevance of specific neural solutions to computational problems that are related to the control of the jamming avoidance response. Some of the recent insights that have emerged from this work include descriptions of mechanisms underlying dynamic receptive field properties, descriptions of the neural activity related to simultaneously occurring sensory stimuli, and a greater understanding of the role of short-term synaptic plasticity in temporal processing.

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.