Packet information encoding in a cerebellum-like circuit.

Packet information encoding of neural signals was proposed for vision about 50 years ago and has recently been revived as a plausible strategy generalizable to natural and artificial sensory systems. It involves discrete image segmentation controlled by feedback and the ability to store and compare packets of information. This article shows that neurons of the cerebellum-like electrosensory lobe (EL) of the electric fish Gymnotus omarorum use spike-count and spike-timing distribution as constitutive variables of packets of information that encode one-by-one the electrosensory images generated by a self-timed series of electric organ discharges (EODs). To evaluate this hypothesis, extracellular unitary activity was recorded from the centro-medial map of the EL. Units recorded in high-decerebrate preparations were classified into six types using hierarchical cluster analysis of post-EOD spiking histograms. Cross-correlation analysis indicated that each EOD strongly influences the unit firing probability within the next inter-EOD interval. Units of the same type were similarly located in the laminar organization of the EL and showed similar stimulus-specific changes in spike count and spike timing after the EOD when a metal object was moved close by, along the fish's body parallel to the skin, or when the longitudinal impedance of a static cylindrical probe placed at the center of the receptive field was incremented in a stepwise manner in repetitive trials. These last experiments showed that spike-counts and the relative entropy, expressing a comparative measure of information before and after the step, were systematically increased with respect to a control in all unit types. The post-EOD spike-timing probability distribution and the relatively independent contribution of spike-timing and number to the content of information in the transmitted packet suggest that these are the constitutive image-encoding variables of the packets. Comparative analysis suggests that packet information transmission is a general principle for processing superposition images in cerebellum-like networks.

Getting the news in milliseconds: The role of early novelty detection in active electrosensory exploration.

The pulse emitting weakly electric fish Gymnotus omarorum shows stereotyped "novelty responses" consisting of a transient acceleration of the rhythm of a self-emitted electric organ discharge that carries electrosensory signals. Here we show that rapid increases in electric image amplitude cause a "novelty detection potential" in the first electrosensory relay. This sign precedes and its amplitude predicts, the amplitude of the subsequent behavioral novelty response. Current source density analyses indicates its origin ar the layers of the electrosensory lobe where the main output neurons occur. Two types of units, referred to as "ON" and "OFF". Were recorded there in decerebrated fish. Firing probability of "OFF" units drastically decreased after a stepwise increase in electric image. By contrast, the very first novel stimuli after the increase evoked a sharp peak in firing rate of "ON" units followed by a very fast adaptation phase that contrasted with the slow adaptation observed in previous recordings of primary afferents. The amplitudes of this peak, the novelty detection potential, and the behavioral novelty responses, show the same dependence on the departure of the newest stimulus intensity from the weighted average of preceding ones suggesting that the signals encoded by "ON" neurons underlay the novelty detection potential, propagates through the hierarchical organization of the electromotor control, and finally contribute to accelerate the electric organ discharge rate. This suggests that detecting novelty at the very early processing stage of electrosensory signals is essential to adapt the electrosensory sampling rate to exploration requirements as they change dynamically.

Waveform sensitivity of electroreceptors in the pulse-type weakly electric fish Gymnotus omarorum.

As in most sensory systems, electrosensory images in weakly electric fish are encoded in two parallel pathways, fast and slow. From work on wave-type electric fish, these fast and slow pathways are thought to encode the time and amplitude of electrosensory signals, respectively. The present study focuses on the primary afferents giving origin to the slow path of the pulse-type weakly electric fish Gymnotus omarorum We found that burst duration coders respond with a high-frequency train of spikes to each electric organ discharge. They also show high sensitivity to phase-frequency distortions of the self-generated local electric field. We explored this sensitivity by manipulating the longitudinal impedance of a probe cylinder to modulate the stimulus waveform, while extracellularly recording isolated primary afferents. Resistive loads only affect the amplitude of the re-afferent signals without distorting the waveform. Capacitive loads cause large waveform distortions aside from amplitude changes. Stepping from a resistive to a capacitive load in such a way that the stimulus waveform was distorted, without changing its total energy, caused strong changes in latency, inter-spike interval and number of spikes of primary afferent responses. These burst parameters are well correlated suggesting that they may contribute synergistically in driving downstream neurons. This correlation also suggests that each receptor encodes a single parameter in the stimulus waveform. The finding of waveform distortion sensitivity is relevant because it may contribute to: (a) enhance electroreceptive range in the peripheral 'electrosensory field', (b) a better identification of living prey at the 'foveal electrosensory field' and (c) detect the presence and orientation of conspecifics. Our results also suggest a revision of the classical view of amplitude and time encoding by fast and slow pathways in pulse-type electric fish.

Electric organ discharges and near-field spatiotemporal patterns of the electromotive force in a sympatric assemblage of Neotropical electric knifefish.

Descriptions of the head-to-tail electric organ discharge (ht-EOD) waveform - typically recorded with electrodes at a distance of approximately 1-2 body lengths from the center of the subject - have traditionally been used to characterize species diversity in gymnotiform electric fish. However, even taxa with relatively simple ht-EODs show spatiotemporally complex fields near the body surface that are determined by site-specific electrogenic properties of the electric organ and electric filtering properties of adjacent tissues and skin. In Brachyhypopomus, a pulse-discharging genus in the family Hypopomidae, the regional characteristics of the electric organ and the role that the complex 'near field' plays in communication and/or electrolocation are not well known. Here we describe, compare, and discuss the functional significance of diversity in the ht-EOD waveforms and near-field spatiotemporal patterns of the electromotive force (emf-EODs) among a species-rich sympatric community of Brachyhypopomus from the upper Amazon.

The slow pathway in the electrosensory lobe of Gymnotus omarorum: field potentials and unitary activity.

This is a first communication on the self-activation pattern of the electrosensory lobe in the pulse weakly electric fish Gymnotus omarorum. Field potentials in response to the fish's own electric organ discharge (EOD) were recorded along vertical tracks (50µm step) and on a transversal lattice array across the electrosensory lobe (resolution 50µm×100µm). The unitary activity of 82 neurons was recorded in the same experiments. Field potential analysis indicates that the slow electrosensory path shows a characteristic post-EOD pattern of activity marked by three main events: (i) a small and early component at about 7ms, (ii) an intermediate peak about 13ms and (iii) a late broad component peaking after 20ms. Unit firing rate showed a wide range of latencies between 3 and 30ms and a variable number of spikes (median 0.28units/EOD). Conditional probability analysis showed monomodal and multimodal post-EOD histograms, with the peaks of unit activity histograms often matching the timing of the main components of the field potentials. Monomodal responses were sub-classified as phase locked monomodal (variance smaller than 1ms), early monomodal (intermediate variance, often firing in doublets, peaking range 10-17ms) and late monomodal (large variance, often firing two spikes separated about 10ms, peaking beyond 17ms). The responses of multimodal units showed that their firing probability was either enhanced, or depressed just after the EOD. In this last (depressed) subtype of unit the probability stepped down just after the EOD. Early inhibition and the presence of early phase locked units suggest that the observed pattern may be influenced by a fast feed forward inhibition. We conclude that the ELL in pulse gymnotiformes is activated in a complex sequence of events that reflects the ELL network connectivity.

On the haptic nature of the active electric sense of fish.

Electroreception is a sensory modality present in chondrichthyes, actinopterygii, amphibians, and mammalian monotremes. The study of this non-intuitive sensory modality has provided insights for better understanding of sensory systems in general and inspired the development of innovative artificial devices. Here we review evidence obtained from the analysis of electrosensory images, neurophysiological data from the recording of unitary activity in the electrosensory lobe, and psychophysical data from analysis of novelty responses provoked in well-defined stimulus conditions, which all confirm that active electroreception has a short range, and that the influence of exploratory movements on object identification is strong. In active electric images two components can be identified: a "global" image profile depending on the volume, shape and global impedance of an object and a "texture" component depending on its surface attributes. There is a short range of the active electric sense and the progressive "blurring" of object image with distance. Consequently, the lack of precision regarding object location, considered together, challenge the current view of this sense as serving long range electrolocation and the commonly used metaphor of "electric vision". In fact, the active electric sense shares more commonalities with human active touch than with teleceptive senses as vision or audition. Taking into account that other skin exteroceptors and proprioception may be congruently stimulated during fish exploratory movements we propose that electric, mechanoceptive and proprioceptive sensory modalities found in electric fish could be considered together as a single haptic sensory system. This article is part of a Special Issue entitled Neural Coding 2012.

Waveform diversity of electric organ discharges: the role of electric organ auto-excitability in Gymnotus spp.

This article shows that differences in the waveforms of the electric organ discharges (EODs) from two taxa are due to the different responsiveness of their electric organs (EOs) to their previous activity (auto-excitability). We compared Gymnotus omarorum endemic to Uruguay (35 degrees South, near a big estuary), which has four components in the head to tail electric field (V(1) to V(4)), with Gymnotus sp. endemic to the south of Brazil, Paraguay and Argentinean Mesopotamia (25 degrees South, inland), which shows a fifth component in addition to the others (V(5)). We found that: (a) the innervation pattern of the electrocytes, (b) the three earlier, neurally driven, EOD components (V(1) to V(3)), and (c) their remnants after curarisation were almost identical in the two taxa. The equivalent electromotive forces of late components (V(4) and V(5)) increased consistently as a function of the external current associated with the preceding component and were abolished by partial curarisation in both taxa. Taken together these data suggest that these components are originated in the responses of the electrocytes to longitudinal currents through the EO. By using a differential load procedure we showed that V(4) in G. omarorum responded to experimental changes in its excitation current with larger amplitude variations than V(4) in Gymnotus sp. We conclude that the differences in the EOD phenotype of the two studied taxa are due to the different EO auto-excitability. This, in turn, is caused either by the different expression of a genetic repertoire of conductance in the electrocyte membrane or in the wall of the tubes forming the EO.

Waveform generation in the weakly electric fish Gymnotus coropinae (Hoedeman): the electric organ and the electric organ discharge.

This article deals with the electric organ and its discharge in Gymnotus coropinae, a representative species of one of the three main clades of the genus. Three regions with bilateral symmetry are described: (1) subopercular (medial and lateral columns of complex shaped electrocytes); (2) abdominal (medial and lateral columns of cuboidal and fusiform electrocytes); and (3) main [four columns, one dorso-lateral (containing fusiform electrocytes) and three medial (containing cuboidal electrocytes)]. Subopercular electrocytes are all caudally innervated whereas two of the medial subopercular ones are also rostrally innervated. Fusiform electrocytes are medially innervated at the abdominal portion, and at their rostral and caudal poles at the main portion. Cuboidal electrocytes are always caudally innervated. The subopercular portion generates a slow head-negative wave (V(1r)) followed by a head-positive spike (V(3r)). The abdominal and main portions generate a fast tetra-phasic complex (V(2345ct)). Since subopercular components prevail in the near field and the rest in the far field, time coincidence of V(3r) with V(2) leads to different waveforms depending on the position of the receiver. This confirms the splitting hypothesis of communication and exploration channels based on the different timing, frequency band and reach of the regional waveforms. The following hypothesis is compatible with the observed anatomo-functional organization: V(1r) corresponds to the rostral activation of medial subopercular electrocytes and V(3r) to the caudal activation of all subopercular electrocytes; V(2), and part of V(3ct), corresponds to the successive activation of the rostral and caudal poles of dorso-lateral fusiform electrocytes; and V(345ct) is initiated in the caudal face of cuboidal electrocytes by synaptic activation (V(3ct)) and it is completed (V(45ct)) by the successive activation of rostral and caudal faces by the action currents evoked in the opposite face.

Active electroreception in Gymnotus omari: imaging, object discrimination, and early processing of actively generated signals.

Weakly electric fishes "electrically illuminate" the environment in two forms: pulse fishes emit a succession of discrete electric discharges while wave fishes emit a continuous wave. These strategies are present in both taxonomic groups of weakly electric fishes, mormyrids and gymnotids. As a consequence one can distinguish four major types of active electrosensory strategies evolving in parallel. Pulse gymnotids have an electrolocating strategy common with pulse mormyrids, but brains of pulse and wave gymnotids are alike. The beating strategy associated to other differences in the electrogenic system and electrosensory responses suggests that similar hardware might work in a different mode for processing actively generated electrosensory images. In this review we summarize our findings in pulse gymnotids' active electroreception and outline a primary agenda for the next research.

Species-specific diversity of a fixed motor pattern: the electric organ discharge of Gymnotus.

Understanding fixed motor pattern diversity across related species provides a window for exploring the evolution of their underlying neural mechanisms. The electric organ discharges of weakly electric fishes offer several advantages as paradigmatic models for investigating how a neural decision is transformed into a spatiotemporal pattern of action. Here, we compared the far fields, the near fields and the electromotive force patterns generated by three species of the pulse generating New World gymnotiform genus Gymnotus. We found a common pattern in electromotive force, with the far field and near field diversity determined by variations in amplitude, duration, and the degree of synchronization of the different components of the electric organ discharges. While the rostral regions of the three species generate similar profiles of electromotive force and local fields, most of the species-specific differences are generated in the main body and tail regions of the fish. This causes that the waveform of the field is highly site dependant in all the studied species. These findings support a hypothesis of the relative separation of the electrolocation and communication carriers. The presence of early head negative waves in the rostral region, a species-dependent early positive wave at the caudal region, and the different relationship between the late negative peak and the main positive peak suggest three points of lability in the evolution of the electrogenic system: a) the variously timed neuronal inputs to different groups of electrocytes; b) the appearance of both rostrally and caudally innervated electrocytes, and c) changes in the responsiveness of the electrocyte membrane.

Post-natal development of the electromotor system in a pulse gymnotid electric fish.

Some fish emit electric fields generated by the coordinated activation of electric organs. Such discharges are used for exploring the environment and for communication. This article deals with the development of the electric organ and its discharge in Gymnotus, a pulse genus in which brief discharges are separated by regular silent intervals. It is focused on the anatomo-functional study of fish sized between 10 and 300 mm from the species of Gymnotus, in which electrogenic mechanisms are best known. It was shown that: (1) electroreception and electromotor control is present from early larval stages; (2) there is a single electric organ from larval to adult stages; (3) pacemaker rhythmicity becomes similar to that of the adult when the body length becomes greater than 45 mm and (4) there is a consistent developmental profile of the electric organ discharge in which waveform components are added according to a programmed sequence. The analysis of these data allowed us to identify three main periods in post-natal development of electrogenesis: (1) before fish reach 55 mm in length, when maturation of neural structures is the main factor determining a characteristic sequence of changes observed in the discharge timing and waveform; (2) between 55 and 100 mm in length, when peripheral maturation of the effector cells and changes in post-effector mechanisms due to the fish's growth determine minor changes in waveform and the increase in amplitude of the discharge and (3) beyond 100 mm in length, when homothetic growth of the fish body explains the continuous increase in electric power of the discharge.