scholarly journals Neural activity in a hippocampus-like region of the teleost pallium are associated with navigation and active sensing

2018 ◽  
Author(s):  
H Fotowat ◽  
C Lee ◽  
JJ Jun ◽  
L Maler
Keyword(s):  
Neural Activity ◽  
Spatial Information ◽  
Electric Organ Discharge ◽  
Discharge Rate ◽  
Spatial Navigation ◽  
Sampling Rate ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Active Sensing ◽  
Head Region

AbstractNeural mechanisms underlying spatial navigation in fish are unknown and little is known, for any vertebrate, about the relationship between active sensing and the formation of spatial maps. The weakly electric fish, Gymnotus Carapo, uses their active electric sense for spatial navigation. The electric organ discharge rate (EODr) undergoes transient increases during navigation to enhance electrosensory sampling. Gymnotus also uses stereotyped forward/ backward swimming as a second form of active sensing that brings objects towards the electroreceptor-dense head region. We wirelessly recorded neural activity from the pallium of freely swimming Gymnotus. Spiking activity was sparse and occurred only during swimming. Notably, some units exhibited significant place specificity and/or association with both forms of active sensing. Our results provide the first characterization of neural activity in a hippocampal-like region of a teleost fish brain and connects active sensing via sensory sampling rate and directed movements to higher order encoding of spatial information.

scholarly journals Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Haleh Fotowat ◽  
Candice Lee ◽  
James Jaeyoon Jun ◽  
Len Maler
Keyword(s):  
Neural Activity ◽  
Electric Organ Discharge ◽  
Discharge Rate ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Active Sensing ◽  
Head Region ◽  
Hippocampal Ca3 ◽  
And Control ◽  
Weakly Electric

Most vertebrates use active sensing strategies for perception, cognition and control of motor activity. These strategies include directed body/sensor movements or increases in discrete sensory sampling events. The weakly electric fish, Gymnotus sp., uses its active electric sense during navigation in the dark. Electric organ discharge rate undergoes transient increases during navigation to increase electrosensory sampling. Gymnotus also use stereotyped backward swimming as an important form of active sensing that brings objects toward the electroreceptor dense fovea-like head region. We wirelessly recorded neural activity from the pallium of freely swimming Gymnotus. Spiking activity was sparse and occurred only during swimming. Notably, most units tended to fire during backward swims and their activity was on average coupled to increases in sensory sampling. Our results provide the first characterization of neural activity in a hippocampal (CA3)-like region of a teleost fish brain and connects it to active sensing of spatial environmental features.

Sensory coding and corollary discharge effects in mormyrid electric fish

1989 ◽  
Vol 146 (1) ◽  
pp. 229-253 ◽  
Author(s):  
C. C. Bell
Keyword(s):  
Electric Fish ◽  
Spatial Information ◽  
Electric Organ Discharge ◽  
Low Frequency ◽  
Electric Organ ◽  
Motor Command ◽  
Corollary Discharge ◽  
Weakly Electric Fish ◽  
Central Projection ◽  
Sensory Coding

Weakly electric fish use their electrosensory systems for electrocommunication, active electrolocation and low-frequency passive electrolocation. In electric fish of the family Mormyridae, these three purposes are mediated by separate classes of electroreceptors: electrocommunication by Knollenorgan electroreceptors, active electrolocation by Mormyromast electroreceptors and low-frequency passive electrolocation by ampullary electroreceptors. The primary afferent fibres from each class of electroreceptors terminate in a separate central region. Thus, the mormyrid electrosensory system has three anatomically and functionally distinct subsystems. This review describes the sensory coding and initial processing in each of the three subsystems, with an emphasis on the Knollenorgan and Mormyromast subsystems. The Knollenorgan subsystem is specialized for the measurement of temporal information but appears to ignore both intensity and spatial information. In contrast, the Mormyromast subsystem is specialized for the measurement of both intensity and spatial information. The morphological and physiological characteristics of the primary afferents and their central projection regions are quite different for the two subsystems and reflect the type of information which the subsystems preserve. This review also describes the electric organ corollary discharge (EOCD) effects which are present in the central projection regions of each of the three electrosensory subsystems. These EOCD effects are driven by the motor command that drives the electric organ to discharge. The EOCD effects are different in each of the three subsystems and these differences reflect differences in both the pattern and significance of the sensory information that is evoked by the fish's own electric organ discharge. Some of the EOCD effects are invariant, whereas others are plastic and depend on previous afferent input. The mormyrid work is placed within two general contexts: (a) the measurement of time and intensity in sensory systems, and (b) the various roles of motor command (efferent) signals and self-induced sensory (reafferent) signals in sensorimotor systems.

scholarly journals Active sensing associated with spatial learning reveals memory-based attention in an electric fish

2016 ◽  
Vol 115 (5) ◽  
pp. 2577-2592 ◽  
Author(s):  
James J. Jun ◽  
André Longtin ◽  
Leonard Maler
Keyword(s):  
Spatial Learning ◽  
Electric Fish ◽  
Electric Organ Discharge ◽  
Distance Sampling ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Active Sensing ◽  
Unit Distance ◽  
Food Location ◽  
Gymnotid Fish

Active sensing behaviors reveal what an animal is attending to and how it changes with learning. Gymnotus sp., a gymnotiform weakly electric fish, generates an electric organ discharge (EOD) as discrete pulses to actively sense its surroundings. We monitored freely behaving gymnotid fish in a large dark “maze” and extracted their trajectories and EOD pulse pattern and rate while they learned to find food with electrically detectable landmarks as cues. After training, they more rapidly found food using shorter, more stereotyped trajectories and spent more time near the food location. We observed three forms of active sensing: sustained high EOD rates per unit distance (sampling density), transient large increases in EOD rate (E-scans) and stereotyped scanning movements (B-scans) were initially strong at landmarks and food, but, after learning, intensified only at the food location. During probe (no food) trials, after learning, the fish's search area and intense active sampling was still centered on the missing food location, but now also increased near landmarks. We hypothesize that active sensing is a behavioral manifestation of attention and essential for spatial learning; the fish use spatial memory of landmarks and path integration to reach the expected food location and confine their attention to this region.

Precision measurement of electric organ discharge timing from freely moving weakly electric fish

2012 ◽  
Vol 107 (7) ◽  
pp. 1996-2007 ◽  
Author(s):  
James J. Jun ◽  
André Longtin ◽  
Leonard Maler
Keyword(s):  
Electric Fish ◽  
Animal Movement ◽  
Electric Organ Discharge ◽  
Discharge Rate ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Central State ◽  
Free Swimming ◽  
Pulse Timing ◽  
Freely Moving

Physiological measurements from an unrestrained, untethered, and freely moving animal permit analyses of neural states correlated to naturalistic behaviors of interest. Precise and reliable remote measurements remain technically challenging due to animal movement, which perturbs the relative geometries between the animal and sensors. Pulse-type electric fish generate a train of discrete and stereotyped electric organ discharges (EOD) to sense their surroundings actively, and rapid modulation of the discharge rate occurs while free swimming in Gymnotus sp. The modulation of EOD rates is a useful indicator of the fish's central state such as resting, alertness, and learning associated with exploration. However, the EOD pulse waveforms remotely observed at a pair of dipole electrodes continuously vary as the fish swims relative to the electrodes, which biases the judgment of the actual pulse timing. To measure the EOD pulse timing more accurately, reliably, and noninvasively from a free-swimming fish, we propose a novel method based on the principles of waveform reshaping and spatial averaging. Our method is implemented using envelope extraction and multichannel summation, which is more precise and reliable compared with other widely used threshold- or peak-based methods according to the tests performed under various source-detector geometries. Using the same method, we constructed a real-time electronic pulse detector performing an additional online pulse discrimination routine to enhance further the detection reliability. Our stand-alone pulse detector performed with high temporal precision (<10 μs) and reliability (error <1 per 106 pulses) and permits longer recording duration by storing only event time stamps (4 bytes/pulse).

Sensitivity to novel feedback at different phases of a gymnotid electric organ discharge

2002 ◽  
Vol 205 (21) ◽  
pp. 3307-3320
Author(s):  
Stefan Schuster ◽  
Natalie Otto
Keyword(s):  
Current Flow ◽  
Electric Organ Discharge ◽  
Discharge Rate ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Spatiotemporal Pattern ◽  
Switch Closure ◽  
Tail Region ◽  
Gymnotid Fish ◽  
Weakly Electric

SUMMARY Weakly electric fish communicate and electrolocate objects in the dark by discharging their electric organs (EOs) and monitoring the spatiotemporal pattern of current flow through their skin. In the South-American pulse-type gymnotid fish these organs often are intriguingly complex, comprising several hundreds of electrogenic cells (electrocytes) of various morphologies,innervation patterns and abilities to generate a spike, distributed over nearly the full length of the fish. An attractive idea is that different parts of the organ may serve distinct functions in electrocommunication and electrolocation. Recent studies support this notion and suggest that the currents produced during the final phase of the electric organ discharge (EOD)are used for communication. Here, we explore a method to directly assess the relevance of the various currents for electrolocation. In this new method, the pattern of current flow during a gymnotid EOD is changed selectively at distinct phases of the EOD so that currents generated by known electrocyte groups are affected. We have studied the roles played by the various currents for the detection of novel feedback at the trunk/tail region of the gymnotid fish Gymnotus carapo. An experimental animal rested in a cage and two electrodes were placed at a close distance to its trunk and tail. An electronic switch briefly connected these electrodes during a selected phase within an EOD and the shunting of EOD current that resulted from switch closure was directly monitored. G. carapo responded with an acceleration of its discharge rate to novelties in the EOD feedback that occurred only for a fraction of a single EOD. Controls in which the switch was closed during the silent intervals between successive EODs showed that the fish responded to the changes in EOD feedback and not to unrelated artefacts of the brief switch closure. Fish responded to shunting of current during all phases; the sensitivity was highest during the final headnegative phase but the magnitude of shunted current was largest in the preceeding phase. The current produced during the final part of the EOD is thus not reserved for communication as previously suggested but plays a predominant role in electrolocation at the trunk and tail region of G. carapo.

Influence of water temperature on the electric organ discharge (EOD) of the weakly electric fish Marcusenius cyprinoides (Mormyridae)

1978 ◽  
Vol 74 (1) ◽  
pp. 133-150 ◽  
Author(s):  
M. J. Toerring ◽  
J. Serrier
Keyword(s):  
Water Temperature ◽  
Electric Organ Discharge ◽  
Discharge Rate ◽  
Natural Habitat ◽  
Central Africa ◽  
Electric Organ ◽  
High Water ◽  
Weakly Electric Fish ◽  
Pulse Interval ◽  
Seasonal Temperature

1. The influence of different water temperatures on the electric organ discharge (EOD) of a mormyrid fish Marcusenius cyprinoides was studied. The range of the water temperatures was fixed according to the seasonal temperature variations of the rivers in Central Africa, the natural habitat of this species. 2. The EOD activity was characterized using the following parameters: mean EOD rate, EOD pattern in the form of Interpulse Interval Histograms (IIH), IIH range, and shortest pulse interval. These parameters remained constant during control experiments at constant temperature (27 degrees C) for 4 days. 3. The mean EOD rate increases with increasing water temperatures. The lowest mean EOD rate is always found at 17 degrees C, the highest between 26 and 33 degrees C. The characteristics of the IIH are modified by stepwise temperature increases. These IIH show during high temperatures (26–33 degrees C) similar patterns to those previously observed during high level motor activity and excitement. The IIH range diminishes with stepwise temperature increases. The shortest pulse interval has a negative, linear correlation with water temperature. 4. The possible role of water temperature in the reproduction of the mormyrids is discussed. The high discharge rate of M. cyprinoides produced by high water temperatures during the rainy season could serve to improve the resolution of the electroreceptors during this period.

scholarly journals A sodium-activated potassium channel supports high-frequency firing and reduces energetic costs during rapid modulations of action potential amplitude

2013 ◽  
Vol 109 (7) ◽  
pp. 1713-1723 ◽  
Author(s):  
Michael R. Markham ◽  
Leonard K. Kaczmarek ◽  
Harold H. Zakon
Keyword(s):  
Action Potential ◽  
High Frequency ◽  
Electric Fish ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Energetic Costs ◽  
Dynamic Regulation ◽  
Voltage Gated

We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) amplitude as a means of regulating energetic costs of AP signaling. Weakly electric fish generate an electric organ discharge (EOD) by summing the APs of their electric organ cells (electrocytes). Some electric fish increase AP amplitude during active periods or social interactions and decrease AP amplitude when inactive, regulated by melanocortin peptide hormones. This modulates signal amplitude and conserves energy. The gymnotiform Eigenmannia virescens generates EODs at frequencies that can exceed 500 Hz, which is energetically challenging. We examined how E. virescens meets that challenge. E. virescens electrocytes exhibit a voltage-gated Na+current ( INa) with extremely rapid recovery from inactivation (τrecov= 0.3 ms) allowing complete recovery of Na+current between APs even in fish with the highest EOD frequencies. Electrocytes also possess an inwardly rectifying K+current and a Na+-activated K+current ( IKNa), the latter not yet identified in any gymnotiform species. In vitro application of melanocortins increases electrocyte AP amplitude and the magnitudes of all three currents, but increased IKNais a function of enhanced Na+influx. Numerical simulations suggest that changing INamagnitude produces corresponding changes in AP amplitude and that KNachannels increase AP energy efficiency (10–30% less Na+influx/AP) over model cells with only voltage-gated K+channels. These findings suggest the possibility that E. virescens reduces the energetic demands of high-frequency APs through rapidly recovering Na+channels and the novel use of KNachannels to maximize AP amplitude at a given Na+conductance.

The electric image in weakly electric fish: perception of objects of complex impedance

2000 ◽  
Vol 203 (3) ◽  
pp. 481-492 ◽  
Author(s):  
R. Budelli ◽  
A.A. Caputi
Keyword(s):  
Linear Function ◽  
Electric Organ Discharge ◽  
Amplitude Ratio ◽  
Complex Impedance ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Peak Amplitude ◽  
Electrical Characteristics ◽  
Electric Image ◽  
Weakly Electric

Weakly electric fish explore the environment using electrolocation. They produce an electric field that is detected by cutaneous electroreceptors; external objects distort the field, thus generating an electric image. The electric image of objects of complex impedance was investigated using a realistic model, which was able to reproduce previous experimental data. The transcutaneous voltage in the presence of an elementary object is modulated in amplitude and waveform on the skin. Amplitude modulation (measured as the relative change in the local peak-to-peak amplitude) consists of a ‘Mexican hat’ profile whose maximum relative slope depends on the distance of the fish from the object. Waveform modulation depends on both the distance and the electrical characteristics of the object. Changes in waveform are indicated by the amplitude ratio of the larger positive and negative phases of the local electric organ discharge on the skin. Using the peak-to-peak amplitude and the positive-to-negative amplitude ratio of this discharge, a perceptual space can be defined and correlated with the capacitance and resistance of the object. When the object is moved away, the perceptual space is reduced but keeps the same proportions (homothetically): for a given object, the positive-to-negative amplitude ratio is a linear function of the peak-to-peak amplitude. This linear function depends on the electrical characteristics of the object. However, there are ‘families’ of objects with different electrical characteristics that produce changes in the parameters of the local electric organ discharge that are related by the same linear function. We propose that these functions code the perceptual properties of an object related to its impedance.

scholarly journals Electric organ discharge patterns during group hunting by a mormyrid fish

2005 ◽  
Vol 272 (1570) ◽  
pp. 1305-1314 ◽  
Author(s):  
Matthew E Arnegard ◽  
Bruce A Carlson
Keyword(s):  
Low Voltage ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Lake Malawi ◽  
Weakly Electric Fish ◽  
Species Flock ◽  
Unexpected Finding ◽  
Size Estimation ◽  
Vertebrate Lineage ◽  
Mormyrid Fish

Weakly electric fish emit and receive low-voltage electric organ discharges (EODs) for electrolocation and communication. Since the discovery of the electric sense, their behaviours in the wild have remained elusive owing to their nocturnal habits and the inaccessible environments in which they live. The transparency of Lake Malawi provided the first opportunity to simultaneously observe freely behaving mormyrid fish and record their EODs. We observed a piscivorous mormyrid, Mormyrops anguilloides , hunting in small groups in Lake Malawi while feeding on rock-frequenting cichlids of the largest known vertebrate species flock. Video recordings yielded the novel and unexpected finding that these groups resembled hunting packs by being largely composed of the same individuals across days. We show that EOD accelerations accompany prey probing and size estimation by M. anguilloides . In addition, group members occasionally synchronize bursts of EODs with an extraordinary degree of precision afforded by the mormyrid echo response. The characteristics and context of burst synchronization suggest that it may function as a pack cohesion signal. Our observations highlight the potential richness of social behaviours in a basal vertebrate lineage, and provide a framework for future investigations of the neural mechanisms, behavioural rules and ecological significance of social predation in M. anguilloides .

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