Phantoms in the brain: Ambiguous representations of stimulus amplitude and timing in weakly electric fish

In wave-type weakly electric fish, two distinct types of primary afferent fibers are specialized for separately encoding modulations in the amplitude and phase (timing) of electrosensory stimuli. Time-coding afferents phase lock to periodic stimuli and respond to changes in stimulus phase with shifts in spike timing. Amplitude-coding afferents fire sporadically to periodic stimuli. Their probability of firing in a given cycle, and therefore their firing rate, is proportional to stimulus amplitude. However, the spike times of time-coding afferents are also affected by changes in amplitude; similarly, the firing rates of amplitude-coding afferents are also affected by changes in phase. Because identical changes in the activity of an individual primary afferent can be caused by modulations in either the amplitude or phase of stimuli, there is ambiguity regarding the information content of primary afferent responses that can result in ‘phantom’ modulations not present in an actual stimulus. Central electrosensory neurons in the hindbrain and midbrain respond to these phantom modulations. Phantom modulations can also elicit behavioral responses, indicating that ambiguity in the encoding of amplitude and timing information ultimately distorts electrosensory perception. A lack of independence in the encoding of multiple stimulus attributes can therefore result in perceptual illusions. Similar effects may occur in other sensory systems as well. In particular, the vertebrate auditory system is thought to be phylogenetically related to the electrosensory system and it encodes information about amplitude and timing in similar ways. It has been well established that pitch perception and loudness perception are both affected by the frequency and intensity of sounds, raising the intriguing possibility that auditory perception may also be affected by ambiguity in the encoding of sound amplitude and timing.     

Influence of sound pressure level on the processing of amplitude modulations by auditory neurons of the locust

Typical features of natural sounds are amplitude changes at different time scales. In many species, amplitude modulations constitute decisive cues to recognize communication signals. Since these signals should be recognizable over a broad intensity range, we investigated how the encoding of amplitude modulations by auditory neurons depends on sound pressure level. Identified neurons that represent different processing stages in the locusts’ auditory pathway were stimulated with sinusoidal modulations of a broad band noise carrier, at different intensities, and characteristic parameters of modulation transfer functions (MTFs) were determined. The corner frequencies of temporal MTFs turned out to be independent of intensity for all neurons except one. Furthermore, for none of the neurons investigated corner frequencies were significantly correlated with spike rate, indicating a remarkable intensity invariance of the upper limits of temporal resolution. The shape of the tMTFs changed with increasing intensity from a low-pass to a band-pass for receptors and local neurons, while no consistent change was observed for ascending neurons. The best modulation frequency depended on intensity and spike rate, especially for receptors and local neurons. Remarkably, the adaptation state of some neurons turned out to be independent of the spike rate during the modulation part of the stimulus.     

Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish

The first stage of information processing in the electrosensory system involves the encoding of local changes in transdermal potential into trains of action potentials in primary electrosensory afferent nerve fibers. To develop a quantitative model of this encoding process for P-type (probability-coding) afferent fibers in the weakly electric fish Apteronotus leptorhynchus, we recorded single unit activity from electrosensory afferent axons in the posterior branch of the anterior lateral line nerve and analyzed responses to electronically generated sinusoidal amplitude modulations of the local transdermal potential. Over a range of AM frequencies from 0.1 to 200 Hz, the modulation transfer function of P-type afferents is high-pass in character, with a gain that increases monotonically up to AM frequencies of 100 Hz where it begins to roll off, and a phase advance with a range of 15–60 degrees. Based on quantitative analysis of the observed gain and phase characteristics, we present a computationally efficient model of P-type afferent response dynamics which accurately characterizes changes in afferent firing rate in response to amplitude modulations of the fish's own electric organ discharge over a wide range of AM frequencies relevant to active electrolocation. Accepted: 14 June 1997     

Spatiotemporal burst coding for extracting features of spatiotemporally varying stimuli

Encoding features of spatiotemporally varying stimuli is quite important for understanding the neural mechanisms of various sensory coding. Temporal coding can encode features of time-varying stimulus, and population coding with temporal coding is adequate for encoding spatiotemporal correlation of stimulus features into spatiotemporal activity of neurons. However, little is known about how spatiotemporal features of stimulus are encoded by spatiotemporal property of neural activity. To address this issue, we propose here a population coding with burst spikes, called here spatiotemporal burst (STB) coding. In STB coding, the temporal variation of stimuli is encoded by the precise onset timing of burst spike, and the spatiotemporal correlation of stimuli is emphasized by one specific aspect of burst firing, or spike packet followed by silent interval. To show concretely the role of STB coding, we study the electrosensory system of a weakly electric fish. Weakly electric fish must perceive the information about an object nearby by analyzing spatiotemporal modulations of electric field around it. On the basis of well-characterized circuitry, we constructed a neural network model of the electrosensory system. Here we show that STB coding encodes well the information of object distance and size by extracting the spatiotemporal correlation of the distorted electric field. The burst activity of electrosensory neurons is also affected by feedback signals through synaptic plasticity. We show that the control of burst activity caused by the synaptic plasticity leads to extracting the stimulus features depending on the stimulus context. Our results suggest that sensory systems use burst spikes as a unit of sensory coding in order to extract spatiotemporal features of stimuli from spatially distributed stimuli.     

Modeling the electric image produced by objects with complex impedance in weakly electric fish

Weakly electric fish generate an electric field around their body by electric organ discharge (EOD). By measuring the modulation of the electric field produced by an object in the field these fish are able to accurately locate an object. Theoretical and experimental studies have focused on the amplitude modulations of EODs produced by resistive objects. However, little is known about the phase modulations produced by objects with complex impedance. The fish must be able to detect changes in object impedance to discriminate between food and nonfood objects. To investigate the features of electric images produced by objects with complex impedance, we developed a model that can be used to map the electric field around the fish body. The present model allows us to calculate the spatial distribution of the amplitude and phase shift in an electric image. This is the first study to investigate the changes in amplitude and phase shift of electric images induced by objects with complex impedance in wave-type fish. Using the model, we show that the amplitude of the electric image exhibits a sigmoidal change as the capacitance and resistance of an object are increased. Similarly, the phase shift exhibits a significant change within the object capacitance range of 0.1–100 nF. We also show that the spatial distribution of the amplitude and phase shifts of the electric image resembles a “Mexican hat” in shape for varying object distances and sizes. The spatial distribution of the phase shift and the amplitude was dependent on the object distance and size. Changes in the skin capacitance were associated with a tradeoff relationship between the magnitude of the amplitude and phase shift of the electric image. The specific range of skin capacitance (1–100 nF) allows the receptor afferents to extract object features that are relevant to electrolocation. These results provide a useful basis for the study of the neural mechanisms by which weakly electric fish recognize object features such as distance, size, and impedance.     

Attentional modulation strength in cortical area MT depends on stimulus contrast

The attentional modulation of sensory information processing in the visual system is the result of top-down influences, which can cause a multiplicative modulation of the firing rate of sensory neurons in extrastriate visual cortex, an effect reminiscent of the bottom-up effect of changes in stimulus contrast. This similarity could simply reflect the multiplicity of both effects. But, here we show that in direction-selective neurons in monkey visual cortical area MT, stimulus and attentional effects share a nonlinearity. These neurons show higher response gain for both contrast and attentional changes for intermediate contrast stimuli and smaller gain for low- and high-contrast stimuli. This finding suggests a close relationship between the neural encoding of stimulus contrast and the modulating effect of the behavioral relevance of stimuli.     

Detection of multiple stimulus features forces a trade-off in the pyramidal cell network of a gymnotiform electric fish's electrosensory lateral line lobe

Modification of an existing neural structure to support a second function will produce a trade-off between the two functions if they are in some way incompatible. The trade-off between two such sensory functions is modeled here in pyramidal neurons of the gymnotiform electric fish's medullar electrosensory lateral line lobe (ELL). These neurons detect two electric stimulus features produced when a nearby object interferes with the fish's autogenous electric field: (1) amplitude modulation across a cell's entire receptive field and (2) amplitude variation within a cell's receptive field produced by an object's edge. A model of sensory integration shows that detection of amplitude modulation and enhancement of spatial contrast involve an inherent mechanistic trade-off and that the severity of the trade-off depends on the particular algorithm of sensory integration. Electrophysiology data indicate that of the two algorithms for sensory integration modeled here for the gymnotiform fish Brachyhypopomus pinnicaudatus, the algorithm with the better trade-off function is used. Further, the intrinsic trade-off within single cells has been surmounted by the replication of ELL into multiple electrosensory map segments, each specialized to emphasize different sensory features. Accepted: 14 June 1997     

Information-processing demands in electrosensory and mechanosensory lateral line systems.

The electrosensory and mechanosensory lateral line systems of fish exhibit many common features in their structural and functional organization, both at the sensory periphery as well as in central processing pathways. These two sensory systems also appear to play similar roles in many behavioral tasks such as prey capture, orientation with respect to external environmental cues, navigation in low-light conditions, and mediation of interactions with nearby animals. In this paper, we briefly review key morphological, physiological, and behavioral aspects of these two closely related sensory systems. We present arguments that the information processing demands associated with spatial processing are likely to be quite similar, due largely to the spatial organization of both systems and the predominantly dipolar nature of many electrosensory and mechanosensory stimulus fields. Demands associated with temporal processing may be quite different, however, due primarily to differences in the physical bases of electrosensory and mechanosensory stimuli (e.g. speed of transmission). With a better sense of the information processing requirements, we turn our attention to an analysis of the functional organization of the associated first-order sensory nuclei in the hindbrain, including the medial octavolateral nucleus (MON), dorsal octavolateral nucleus (DON), and electrosensory lateral line lobe (ELL). One common feature of these systems is a set of neural mechanisms for improving signal-to-noise ratios, including mechanisms for adaptive suppression of reafferent signals. This comparative analysis provides new insights into how the nervous system extracts biologically significant information from dipolar stimulus fields in order to solve a variety of behaviorally relevant problems faced by aquatic animals.     

Temporal processing and adaptation in the songbird auditory forebrain

Songbird auditory neurons must encode the dynamics of natural sounds at many volumes. We investigated how neural coding depends on the distribution of stimulus intensities. Using reverse-correlation, we modeled responses to amplitude-modulated sounds as the output of a linear filter and a nonlinear gain function, then asked how filters and nonlinearities depend on the stimulus mean and variance. Filter shape depended strongly on mean amplitude (volume): at low mean, most neurons integrated sound over many milliseconds, while at high mean, neurons responded more to local changes in amplitude. Increasing the variance (contrast) of amplitude modulations had less effect on filter shape but decreased the gain of firing in most cells. Both filter and gain changes occurred rapidly after a change in statistics, suggesting that they represent nonlinearities in processing. These changes may permit neurons to signal effectively over a wider dynamic range and are reminiscent of findings in other sensory systems.     

Single unit responses in the auditory center of the frog mesencephalon to amplitude-modulated tones

Responses of most single neurons of the torus semicircularis ofRana ridibunda to stimuli of characteristic frequency and with low (10–30%) sinusoidal amplitude modulation were considerably stronger than those of the same neurons to pure tones. Analysis of phase histograms synchronized with the period of modulation was used to study dependence of the response on the frequency of modulation. In some cells the degree of modulation of the phase histogram fell steadily with an increase in modulation frequency, but in others a maximum was found in the 10–20 Hz region. Usually modulations of the phase histogram were significantly greater than stimulus modulation. The phase angle between the maximum of stimulus amplitude and the maximum of the unit response increased as an approximately linear function of the increase in modulation frequency.N. N. Andreev Acoustic Institute, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 12, No. 3, pp. 264–271, May–June, 1980.     

Distinct neuronal types contribute to hybrid temporal encoding strategies in primate auditory cortex

Studies of the encoding of sensory stimuli by the brain often consider recorded neurons as a pool of identical units. Here, we report divergence in stimulus-encoding properties between subpopulations of cortical neurons that are classified based on spike timing and waveform features. Neurons in auditory cortex of the awake marmoset (Callithrix jacchus) encode temporal information with either stimulus-synchronized or nonsynchronized responses. When we classified single-unit recordings using either a criteria-based or an unsupervised classification method into regular-spiking, fast-spiking, and bursting units, a subset of intrinsically bursting neurons formed the most highly synchronized group, with strong phase-locking to sinusoidal amplitude modulation (SAM) that extended well above 20 Hz. In contrast with other unit types, these bursting neurons fired primarily on the rising phase of SAM or the onset of unmodulated stimuli, and preferred rapid stimulus onset rates. Such differentiating behavior has been previously reported in bursting neuron models and may reflect specializations for detection of acoustic edges. These units responded to natural stimuli (vocalizations) with brief and precise spiking at particular time points that could be decoded with high temporal stringency. Regular-spiking units better reflected the shape of slow modulations and responded more selectively to vocalizations with overall firing rate increases. Population decoding using time-binned neural activity found that decoding behavior differed substantially between regular-spiking and bursting units. A relatively small pool of bursting units was sufficient to identify the stimulus with high accuracy in a manner that relied on the temporal pattern of responses. These unit type differences may contribute to parallel and complementary neural codes.

Neurons in auditory cortex show highly diverse responses to sounds. This study suggests that neuronal type inferred from baseline firing properties accounts for much of this diversity, with a subpopulation of bursting units being specialized for precise temporal encoding.     

To Burst or Not to Burst?

It is well known that some neurons tend to fire packets of action potentials followed by periods of quiescence (bursts) while others within the same stage of sensory processing fire in a tonic manner. However, the respective computational advantages of bursting and tonic neurons for encoding time varying signals largely remain a mystery. Weakly electric fish use cutaneous electroreceptors to convey information about sensory stimuli and it has been shown that some electroreceptors exhibit bursting dynamics while others do not. In this study, we compare the neural coding capabilities of tonically firing and bursting electroreceptor model neurons using information theoretic measures. We find that both bursting and tonically firing model neurons efficiently transmit information about the stimulus. However, the decoding mechanisms that must be used for each differ greatly: a non-linear decoder would be required to extract all the available information transmitted by the bursting model neuron whereas a linear one might suffice for the tonically firing model neuron. Further investigations using stimulus reconstruction techniques reveal that, unlike the tonically firing model neuron, the bursting model neuron does not encode the detailed time course of the stimulus. A novel measure of feature detection reveals that the bursting neuron signals certain stimulus features. Finally, we show that feature extraction and stimulus estimation are mutually exclusive computations occurring in bursting and tonically firing model neurons, respectively. Our results therefore suggest that stimulus estimation and feature extraction might be parallel computations in certain sensory systems rather than being sequential as has been previously proposed.     

Modulation of sensorimotor pathways associated with gain changes in a posture-control network of an insect

The resistance reflex in the femur-tibia joint of stick insects shows a great variability in its strength which allows the animal to adapt to different environmental requirements. This paper presents the modulations in the neural reflex pathways which occur during an increase of the gain of the resistance reflex after tactile stimulation. The gain increase was associated with a short-term, reversible increase of slow extensor tibiae depolarization. Because membrane properties like resting potential and input resistance of this motoneuron remained unchanged during the gain changes, the increase of depolarization appeared to result from an increase of stimulus-related inputs and thus was due to modulations of the premotor neuronal network containing afferents of the femoral chordotonal organ and interneurons. However, no changes of spike activity of sensory neurons and amount of their presynaptic inhibition was found during gain changes. In contrast, recordings from different types of identified premotor non-spiking interneurons demonstrated a correlation between the amplitude of stimulus-related inputs to particular non-spiking interneurons and gain changes, while other non-spiking interneurons appeared unaffected. Thus, an increase in gain of the resistance reflex must be due to a specific weighting of synapses between sense organ and particular non-spiking interneurons. Accepted: 3 July 1998     

Olfactory inputs to hypothalamic neurons controlling reproduction and fertility

In order to gain insight into sensory processing modulating reproductive behavioral and endocrine changes, we have aimed at identifying afferent pathways to neurons synthesizing luteinizing hormone-releasing hormone (LHRH, also known as gonadotropin-releasing hormone [GnRH]), a key neurohormone of reproduction. Injection of conditional pseudorabies virus into the brain of an LHRH::CRE mouse line led to the identification of neuronal networks connected to LHRH neurons. Remarkably, and in contrast to established notions on the nature of LHRH neuronal inputs, our data identify major olfactory projection pathways originating from a discrete population of olfactory sensory neurons but fail to document any synaptic connectivity with the vomeronasal system. Accordingly, chemosensory modulation of LHRH neuronal activity and mating behavior are dramatically impaired in absence of olfactory function, while they appear unaffected in mouse mutants lacking vomeronasal signaling. Further visualization of afferents to LHRH neurons across the brain offers a unique opportunity to uncover complex polysynaptic circuits modulating reproduction and fertility.     

Sex recognition and neuronal coding of electric organ discharge waveform in the pulse-type weakly electric fish, Hypopomus occidentalis

1. Hypopomus occidentalis, a weakly electric gymnotiform fish with a pulse-type discharge, has a sexually dimorphic electric organ discharge (Hagedorn 1983). The electric organ discharges (EODs) of males in the breeding season are longer in duration and have a lower peak-power frequency than the EODs of females. We tested reproductively mature fish in the field by presenting electronically generated stimuli in which the only cue for sex recognition was the waveshape of individual EOD-like pulses in a train. We found that gravid females could readily discriminate male-like from female-like EOD waveshapes, and we conclude that this feature of the electric signal is sufficient for sex recognition. 2. To understand the possible neural bases for discrimination of male and female EODs by H . occidentalis, we conducted a neurophysiological examination of both peripheral and central neurons. Our studies show that there are sets of neurons in this species which can discriminate male or female EODs by coding either temporal or spectral features of the EOD. 3. Temporal encoding of stimulus duration was observed in evoked field potential recordings from the magnocellular nucleus of the midbrain torus semicircularis. This nucleus indirectly receives pulse marker electroreceptor information. The field potentials suggest that comparison is possible between pulse marker activity on opposite sides of the body. 4. From standard frequency-threshold curves, spectral encoding of stimulus peak-power frequency was measured in burst duration coder electroreceptor afferents. In both male and female fish, the best frequencies of the narrow-band population of electroreceptors were lower than the peak-power frequency of the EOD. Based on this observation, and the presence of a population of wide-band receptors which can serve as a frequency-independent amplitude reference, a slope-detection model of frequency discrimination is advanced. 5. Spectral discrimination of EOD peak-power frequency was also shown to be possible in a more natural situation similar to that present during behavioral discrimination. As the fish's EOD mimic slowly scanned through and temporally coincided with the neighbor's EOD mimic, peak spike rate in burst duration coder afferents was measured. Spike rate at the moment of coincidence changed predictably as a function of the neighbor's EOD peak-power frequency. 6. Single-unit threshold measurements were made on afferents from peripheral burst duration coder receptors in the amplitude-coding pathway, and midbrain giant cells in the time-coding pathway.(ABSTRACT TRUNCATED AT 400 WORDS)     

Modulation of visual physiology by behavioral state in monkeys, mice, and flies

When a monkey attends to a visual stimulus, neurons in visual cortex respond differently to that stimulus than when the monkey attends elsewhere. In the 25 years since the initial discovery, the study of attention in primates has been central to understanding flexible visual processing. Recent experiments demonstrate that visual neurons in mice and fruit flies are modulated by locomotor behaviors, like running and flying, in a manner that resembles attention-based modulations in primates. The similar findings across species argue for a more generalized view of state-dependent sensory processing and for a renewed dialogue among vertebrate and invertebrate research communities.     

Corticothalamic feedback and sensory processing

Although nearly half of the synaptic input to neurons in the dorsal thalamus comes from the cerebral cortex, the role of corticothalamic projections in sensory processing remains elusive. Although sensory afferents certainly establish the basic receptive field properties of thalamic neurons, increasing evidence indicates that feedback from the cortex plays a crucial role in shaping thalamic responses. Here, we review recent work on the corticothalamic pathways associated with the visual, auditory, and somatosensory systems. Collectively, these studies demonstrate that sensory responses of thalamic neurons result from dynamic interactions between feedforward and feedback pathways.     

Sparsity and Compressed Coding in Sensory Systems

Considering that many natural stimuli are sparse, can a sensory system evolve to take advantage of this sparsity? We explore this question and show that significant downstream reductions in the numbers of neurons transmitting stimuli observed in early sensory pathways might be a consequence of this sparsity. First, we model an early sensory pathway using an idealized neuronal network comprised of receptors and downstream sensory neurons. Then, by revealing a linear structure intrinsic to neuronal network dynamics, our work points to a potential mechanism for transmitting sparse stimuli, related to compressed-sensing (CS) type data acquisition. Through simulation, we examine the characteristics of networks that are optimal in sparsity encoding, and the impact of localized receptive fields beyond conventional CS theory. The results of this work suggest a new network framework of signal sparsity, freeing the notion from any dependence on specific component-space representations. We expect our CS network mechanism to provide guidance for studying sparse stimulus transmission along realistic sensory pathways as well as engineering network designs that utilize sparsity encoding.     

Spatial cueing,sensory gating and selective response preparation: an ERP study on visuo-spatial orienting

Event-related brain potentials (ERPs) were recorded in a visuo-spatial attention task where the position of an imperative stimulus was indicated either validly or invalidly by a central arrow (trial-by-trial cueing). Subjects had to perform choice RT tasks with the response being dependent either on the identity of the target stimulus or on its position. When target identity was relevant for response selection, validly cued stimuli elicited amplitude enhancements of the early, sensory-evoked P1 and N1 components at lateral posterior sites. The N1 validity effect was limited to scalp sites ipsilateral to the visual field of stimulus presentation. Although these effects were found only when the sensory discrimination task was considerably difficult, they are in line with models assuming that modulations of sensory-perceptual processing (“sensory gating”) are induced by spatial cueing. However, when target location was response-relevant, N1 amplitude enhancements were consistently elicited by invalidly cued letters.CNV and LRP measures indicated that the arrow elicited response-related processing in the cue-target interval. Such processes occurred even when the cue contained no information about an upcoming response. Two consecutive lateralization phases were distinguishable in the LRP, with experimentally induced response assignments becoming effective only during the second phase.