Joseph Bastian

The Generation and Subtraction of Sensory Expectations within Cerebellum-Like Structures

The generation of expectations about sensory input and the subtraction of such expectations from actual input appear to be important features of sensory processing. This paper describes the generation of sensory expectations within cerebellum-like structures of four distinct groups of fishes: Mormyridae; Rajidae; Scorpaenidae; and Apteronotidae. These structures consist of a sheet-like array of principal cells. Apical dendrites of the principal cells extend out into a molecular layer where they are contacted by parallel fibers. The basilar regions of the arrays receive primary afferent input from octavolateral endorgans, i.e., electroreceptors, mechanical lateral line neuromasts, or eighth nerve endorgans. The parallel fibers in the molecular layer convey various types of information, including corollary discharge signals associated with motor commands, sensory information from other modalities such as proprioception, and descending input from higher stages of the sensory modality that is processed by the structure. Associations between the signals conveyed by the parallel fibers and particular patterns of sensory input to the basal layers lead to the generation of a negative image of expected sensory input within the principal cell array. Addition of this negative image to actual sensory input results in the subtraction of expected from actual input, allowing the unexpected or novel input to stand out more clearly. Intracellular recording indicates that the negative image is probably generated by means of anti-Hebbian synaptic plasticity at the parallel fiber to principal cell synapse. The results are remarkably similar in the different fishes and may generalize to cerebellum-like structures in other sensory systems and taxa.

Non-classical receptive field mediates switch in a sensory neuron's frequency tuning.

Animals have developed stereotyped communication calls to which specific sensory neurons are well tuned. These communication calls must be discriminated from environmental signals such as those produced by prey. Sensory systems might have evolved neural circuitry to encode both categories. In weakly electric fish, prey and communication signals differ in their spatial extent and frequency content. Here we show that stimuli of different spatial extents mimicking prey and communication signals cause a switch in the frequency tuning and spike-timing precision of electrosensory pyramidal neurons, resulting in the selective and optimal encoding of both stimulus categories. As in other sensory systems, pyramidal neurons respond only to stimuli located within a restricted region of space known as the classical receptive field (CRF). In some systems, stimulation outside the CRF but within a non-classical receptive field (nCRF) can modulate the neural response to CRF stimulation even though nCRF stimulation alone fails to elicit responses. We show that pyramidal neurons possess a nCRF and that it can modulate the response to CRF stimuli to induce this neurobiological switch in frequency tuning.

Parallel processing of sensory input by bursts and isolated spikes.

Burst firing is commonly observed in many sensory systems and is proposed to transmit information reliably. Although a number of biophysical burst mechanisms have been identified, the relationship between burst dynamics and information transfer is uncertain. Electrosensory pyramidal cells have a well defined backpropagation-dependent burst mechanism. We used in vivo, in vitro, and modeling approaches to investigate pyramidal cell responses to mimics of behaviorally relevant sensory input. We found that within a given spike train, bursts are biased toward low-frequency events while isolated spikes simultaneously code for the entire frequency range. We also demonstrated that burst dynamics are essential for optimal feature detection but are not required for stimulus estimation. We conclude that burst and spike dynamics can segregate a single spike train into two parallel and complementary streams of information transfer.

Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli

Stimulus-induced oscillations occur in visual, olfactory and somatosensory systems. Several experimental and theoretical studies have shown how such oscillations can be generated by inhibitory connections between neurons. But the effects of realistic spatiotemporal sensory input on oscillatory network dynamics and the overall functional roles of such oscillations in sensory processing are poorly understood. Weakly electric fish must detect electric field modulations produced by both prey (spatially localized) and communication (spatially diffuse) signals. Here we show, through in vivo recordings, that sensory pyramidal neurons in these animals produce an oscillatory response to communication-like stimuli, but not to prey-like stimuli. On the basis of well-characterized circuitry, we construct a network model of pyramidal neurons that predicts that diffuse delayed inhibitory feedback is required to achieve oscillatory behaviour only in response to communication-like stimuli. This prediction is experimentally verified by reversible blockade of feedback inhibition that removes oscillatory behaviour in the presence of communication-like stimuli. Our results show that a sensory system can use inhibitory feedback as a mechanism to ‘toggle’ between oscillatory and non-oscillatory firing states, each associated with a naturalistic stimulus.

The physiology and morphology of two types of electrosensory neurons in the weakly electric fishApteronotus leptorhynchus

SummaryPrevious anatomical and physiological studies of the gymnotoid electrosensory lateral line lobe (ELLL) suggest that the anatomically identified basilar and non-basilar pyramidal cells correspond to the physiologically defined E and I cells. Intracellular injection of horseradish peroxidase (HRP) into physiologically identified E and I cells confirms this hypothesis. The morphologies and physiological responses of the basilar and non-basilar pyramidal cells were compared. Both types of pyramidal cells have extensive apical dendritic trees that interact with a parallel fiber network in the ELLL. The apical dendritic trees of the non-basilar pyramidal cells have a wider spread along the rostrocaudal axis of the ELLL than those of the basilar pyramidal cells. This difference is discussed in reference to the interaction of these cell types with the parallel fibers of the ELLL. The density of apical dendritic branches was measured and related to the distance of these branches from the cell body. No obvious differences were seen between the dendritic density patterns of basilar and non-basilar pyramidal cells. An interesting correlation, however, exists between the atypical physiological characteristics of two basilar pyramidal cells and their dendritic density patterns. Two cells of the medial (ampullary) segment of the ELLL were analyzed. Like the pyramidal cells of the three lateral (tuberous) regions of the ELLL, the physiology of these cells appears to be related to the presence of an extended basilar process. The ampullary cells, however, have apical dendritic trees that are oriented orthogonally to the dendritic trees of the pyramidal cells.

Electroreceptor neuron dynamics shape information transmission.

The gymnotiform weakly electric fish Apteronotus leptorhynchus can capture prey using electrosensory cues that are dominated by low temporal frequencies. However, conventional tuning curves predict poor electroreceptor afferent responses to low-frequency stimuli. We compared conventional tuning curves with information tuning curves and found that the latter predicted substantially improved responses to these behaviorally relevant stimuli. Analysis of receptor afferent baseline activity showed that negative correlations reduced low-frequency noise levels, thereby increasing information transmission. Multiunit recordings from receptor afferents showed that this increased information transmission could persist at the population level. Finally, we verified that this increased low-frequency information is preserved in the spike trains of central neurons that receive receptor afferent input. Our results demonstrate that conventional tuning curves can be misleading when certain noise reduction strategies are used by the nervous system.

Pyramidal-cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs

Recordings within the posterior eminentia granularis of the weakly electric fish, Apteronotus leptorhynchus, revealed multiple types of proprioceptive units responsive to changes in the position of the animals trunk and tail. Intracellular labelling showed that the proprioceptor recordings were made from axons that ramify extensively within the EGp. The location of the somata giving rise to these axons is presently unknown. Electroreceptor afferent responses to electric organ discharge amplitude modulations caused by movement of the animals tail were compared to responses caused by electronically generated AMs of similar amplitude and time course. These did not differ. Electrosensory lateral line lobe pyramidal cells responded significantly less to electric organ discharge amplitude modulations caused by changing the animals posture as compared to electronically produced AMs, suggesting that central mechanisms attenuate pyramidal cell responses to reafferent electrosensory inputs. Experiments in which the pattern of reafferent input associated with changes in posture was altered revealed that the pyramidal cells learn, over a time course of several minutes, to reject new patterns of input. Both proprioceptive input and descending electrosensory input to the posterior eminentia granularis are involved in generating the observed plastic changes in pyramidal cell responsiveness.

Temporal processing across multiple topographic maps in the electrosensory system.

Multiple topographic representations of sensory space are common in the nervous system and presumably allow organisms to separately process particular features of incoming sensory stimuli that vary widely in their attributes. We compared the response properties of sensory neurons within three maps of the body surface that are arranged strictly in parallel to two classes of stimuli that mimic prey and conspecifics, respectively. We used information-theoretic approaches and measures of phase locking to quantify neuronal responses. Our results show that frequency tuning in one of the three maps does not depend on stimulus class. This map acts as a low-pass filter under both conditions. A previously described stimulus-class-dependent switch in frequency tuning is shown to occur in the other two maps. Only a fraction of the information encoded by all neurons could be recovered through a linear decoder. Particularly striking were low-pass neurons the information of which in the high-frequency range could not be decoded linearly. We then explored whether intrinsic cellular mechanisms could partially account for the differences in frequency tuning across maps. Injection of a Ca2+ chelator had no effect in the map with low-pass characteristics. However, injection of the same Ca2+ chelator in the other two maps switched the tuning of neurons from band-pass/high-pass to low-pass. These results show that Ca2+-dependent processes play an important part in determining the functional roles of different sensory maps and thus shed light on the evolution of this important feature of the vertebrate brain.

The control ofEigenmannia's pacemaker by distributed evaluation of electroreceptive afferences

SummaryThis study analyzes the algorithm by which a distributed system of neurons evaluates specific features in sensory feedback and thereby controls a behavioral response.The electric fishEigenmannia raises or lowers the frequency,f1, of its electric organ pacemaker in response to a neighbors frequency,f2, which is slightly lower or higher respectively than its own frequency. This Jamming Avoidance Response (JAR) thus serves to increase the difference in frequencies,Δf=f2−f1, which is necessary to enhance the animals electrolocation ability. The JAR is driven by electroreceptive afferences from the individuals electric organ discharges (EODs) which, in different parts of the body surface, are unevenly contaminated by EODs of the other fish. This can be demonstrated, in an open loop experiment, by replacing the silenced, nearly sinusoidal EODs of a curarized fish by a sine wave stimulus,S1, mixed with a similar stimulus,S2, which mimicks EODs of another fish. The JAR is controlled by joint modulations of instantaneous phase,H, and amplitude, ¦S¦, of the composite signal,S1+S2. These modulations, if plotted in a two-dimensional state-plane withH and ¦S¦ as its axes, form a circular graph whose sense of rotation is counterclockwise for positiveΔfs and clockwise for negativeΔfs. The sense of rotation thus determines the direction in which the pacemaker frequency is to be shifted. Modulations ofH and ¦S¦ are encoded by specialized electroreceptors,T- andP-units respectively (Fig. 1).Applying various forms of artificial computer generated modulations of phase and amplitude, many of which never occur in a natural situation, and by independently stimulating different parts of the curarized animals body surface, we demonstrate the following:1.The animal detects a modulation in phase,H, of the stimulus in an area,A, of its body surface by comparing the arrival time,tA, of signals fromT-units in areaA with the arrival time,tB, of signals fromT-units in a different area,B. Differential contamination of the animals EOD by a foreign EOD in areasA andB will cause a periodic modulation of the interval,tA−tB. No JARs can be elicited without such modulations in at least some parts of the animals body surface.2.Increases as well as decreases of the amplitude, ¦S¦A, of the stimulus in areaA may either accelerate or decelerate the pacemaker, depending upon the momentary value oftA−tB. Amplitude modulations drive the JAR most likely via associated modulations inP-unit activity (Figs. 3–6).3.The mechanism in (2) is such that, with areaA being more heavily contaminated than areaB, the pattern of joint modulations of ¦S¦A andtA−tB accelerates and decelerates the pacemaker for negative and positiveΔfs respectively. The respective modulations, ¦S¦B andtB−tA, in areaB, which yield a graph with a sense of rotation opposite to that in areaA, cause responses which are opposite but smaller in absolute terms than those in areaA. As a consequence, the net effect of this pairwise interaction between areasA andB is a shift in pacemaker frequency in the direction favored by the variables of areaA, ¦S¦A andtA−tB (Figs. 11, 14).4.The JAR thus appears to be driven by a distributed system of pairwise interactions between neighborhoods ofT-units on the animals body surface. These interactions control the effect of local modulations inP-unit activity upon the frequency of the pacemaker. The nature of this system does not require that the animal has any central representation of its own or any neighbors EOD activity. The findings in this paper are based on behavioral experiments on basically intact animals. The subsequent paper treats neuronal correlates of the JAR.

Feedback and Feedforward Control of Frequency Tuning to Naturalistic Stimuli

Sensory neurons must respond to a wide variety of natural stimuli that can have very different spatiotemporal characteristics. Optimal responsiveness to subsets of these stimuli can be achieved by devoting specialized neural circuitry to different stimulus categories, or, alternatively, this circuitry can be modulated or tuned to optimize responsiveness to current stimulus conditions. This study explores the mechanisms that enable neurons within the initial processing station of the electrosensory system of weakly electric fish to shift their tuning properties based on the spatial extent of the stimulus. These neurons are tuned to low frequencies when the stimulus is restricted to a small region within the receptive field center but are tuned to higher frequencies when the stimulus impinges on large regions of the sensory epithelium. Through a combination of modeling and in vivo electrophysiology, we reveal the respective contributions of the filtering characteristics of extended dendritic structures and feedback circuitry to this shift in tuning. Our results show that low-frequency tuning can result from the cable properties of an extended dendrite that conveys receptor-afferent information to the cell body. The shift from low- to high-frequency tuning, seen in response to spatially extensive stimuli, results from increased wide-band input attributable to activation of larger populations of receptor afferents, as well as the activation of parallel fiber feedback from the cerebellum. This feedback provides a cancellation signal with low-pass characteristics that selectively attenuates low-frequency responsiveness. Thus, with spatially extensive stimuli, these cells preferentially respond to the higher-frequency components of the receptor-afferent input.