Recurrent Feedback in the Mormyrid Electrosensory System: Cells of the Preeminential and Lateral Toral Nuclei

2005 ◽  
Vol 93 (4) ◽  
pp. 2090-2103 ◽  
Author(s):  
Nathaniel B. Sawtell ◽  
Claudia Mohr ◽  
Curtis C. Bell
Keyword(s):  
Electric Organ Discharge ◽  
Electric Organ ◽  
Motor Command ◽  
Cell Types ◽  
Electrosensory System ◽  
Mormyrid Fish ◽  
Descending Input ◽  
Initial Description ◽  
Electrosensory Processing ◽  
Direct Feedback

Many sensory regions integrate information ascending from peripheral receptors with descending inputs from other central structures. However, the significance of these descending inputs remains poorly understood. Descending inputs are prominent in the electrosensory system of mormyrid fish and include both recurrent connections from higher to lower stages of electrosensory processing and electric organ corollary discharge (EOCD) signals associated with the motor command that drives the electric organ discharge. The preeminential nucleus (PE) occupies a key position in a feedback loop that returns information from higher stages of electrosensory processing to the initial stage of processing in the electrosensory lobe (ELL). This feedback reflects the integration of ascending electrosensory input from ELL, descending input from the lateral toral nucleus (torus), and EOCD inputs to PE. We used intracellular recording and axonal tracing of stained cells to characterize EOCD and electrosensory responses of several cell types in PE and the torus. PE and toral cells exhibit prominent EOCD responses that are not due to EOCD inputs from ELL. PE cells giving rise to a direct feedback projection to ELL respond to electrosensory stimuli with rapid, precisely timed spikes that will affect ELL neurons early during the same EOD cycle. EOCD and electrosensory responses in toral cells are similar to those observed in PE and may be important in shaping feedback to ELL. These results provide an initial description of electrosensory feedback to ELL as well as information about how ascending, descending, and EOCD inputs are combined at higher stages of electrosensory processing.

Neuronal responses to electrosensory input in mormyrid valvula cerebelli

1978 ◽  
Vol 41 (6) ◽  
pp. 1495-1510 ◽  
Author(s):  
C. J. Russell ◽  
C. C. Bell
Keyword(s):  
Single Unit ◽  
Evoked Potential ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Neuronal Responses ◽  
Sensory Stimuli ◽  
Separate Area ◽  
Mormyrid Fish ◽  
Electrosensory Processing ◽  
Gnathonemus Petersii

1. We have examined a large portion of the valvula cerebelli of the mormyrid fish Gnathonemus petersii for responses related to the three known classes of electroreceptors. Evoked potential and extracellular single-unit records from curarized and non-curarized preparations show that a separate area of the valvula is related to each of the different electrosensory modalities. 2. The area related to ampullary receptors is also strongly affected by mechanical stimulation to the skin. In the mormyromast and Knollenorgan regions, responses to sensory stimuli depend on when they are given in relation to the command to fire the electric organ. In the Knollenorgan region the interaction is quite simple. Responses are completely blocked if the stimulus is given during a brief period when the electric organ discharge occurs. A greater variety of interactions is seen in the mormyromast region. 3. Large areas of the valvula do not appear to be clearly and strongly retated to any of the three electrosensory modalities, suggesting the possibility that much of the structure is not devoted to electrosensory processing.

scholarly journals The Mormyromast Region of the Mormyrid Electrosensory Lobe. I. Responses to Corollary Discharge and Electrosensory Stimuli

2003 ◽  
Vol 90 (2) ◽  
pp. 1193-1210 ◽  
Author(s):  
Claudia Mohr ◽  
Patrick D. Roberts ◽  
Curtis C. Bell
Keyword(s):  
Electric Organ Discharge ◽  
Electric Organ ◽  
Motor Command ◽  
Cell Types ◽  
Corollary Discharge ◽  
Fusiform Cell ◽  
Central Processing ◽  
New Information ◽  
Afferent Fibers ◽  
Primary Afferent Fibers

This is the first of two papers on the electrosensory lobe (ELL) of mormyrid electric fish. The ELL is the first stage in the central processing of electrosensory information from electroreceptors. Cells of the mormyrid ELL are affected at the time of the electric organ discharge (EOD) by two different inputs, EOD-evoked reafferent input from electroreceptors and corollary discharge input associated with the motor command that elicits the EOD. This first paper examines the intracellular responses of ELL cells to these two different inputs in the region of ELL that receives primary afferent fibers from mormyromast electroreceptors. Mormyromast electroreceptors are responsible for active electrolocation. The paper extends previous studies of the mormyrid ELL by describing the physiological responses of cell types, which had been previously identified only morphologically, including: the two types of Purkinje-like medium ganglionic cells, MG1 and MG2; the thick smooth dendrite cells; and the medium fusiform cells. In addition, two previously unrecognized cell types, the large thick smooth dendrite cell and the interzonal cell, are described both morphologically and physiologically for the first time. Finally, new information is provided on the two types of ELL efferent cells, the large ganglionic and large fusiform cells. All cell types, except for the medium fusiform cell, show nonlinear interactions between electrosensory and corollary discharge inputs. All cell types, except for the medium fusiform cell and the interzonal cell, also show plasticity of the corollary discharge response after pairing with electrosensory stimuli.

scholarly journals Plasticity of feedback inputs in the apteronotid electrosensory system

1999 ◽  
Vol 202 (10) ◽  
pp. 1327-1337 ◽  
Author(s):  
J. Bastian
Keyword(s):  
Synaptic Plasticity ◽  
Adaptive Filters ◽  
Electric Fish ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
The Body ◽  
Weakly Electric Fish ◽  
Electrosensory System ◽  
Electrosensory Processing ◽  
Weakly Electric

Weakly electric fish generate an electric field surrounding their body by means of an electric organ typically located within the trunk and tail. Electroreceptors scattered over the surface of the body encode the amplitude and timing of the electric organ discharge (EOD), and central components of the electrosensory system analyze the information provided by the electroreceptor afferents. The electrosensory system is used for electrolocation, for the detection and analysis of objects near the fish which distort the EOD and for electrocommunication. Since the electric organ is typically located in the tail, any movement of this structure relative to the rest of the body alters the EOD field, resulting in large changes in receptor afferent activity. The amplitude of these reafferent stimuli can exceed the amplitudes of near-threshold electrolocation signals by several orders of magnitude. This review summarizes recent studies of the South American weakly electric fish Apteronotus leptorhynchus aimed at determining how the animals differentiate self-generated or reafferent electrosensory stimuli from those that are more behaviorally relevant. Cells within the earliest stages of central electrosensory processing utilize an adaptive filtering technique which allows the system preferentially to attenuate reafferent as well as other predictable patterns of sensory input without degrading responses to more novel stimuli. Synaptic plasticity within the system underlies the adaptive component of the filter and enables the system to learn to reject new stimulus patterns if these become predictable. A Ca2+-mediated form of postsynaptic depression contributes to this synaptic plasticity. The filter mechanism seen in A. leptorhynchus is surprisingly similar to adaptive filters described previously in mormyrid weakly electric fish and in elasmobranchs, suggesting that this mechanism may be a common feature of sensory processing systems.

Sensory processing and corollary discharge effects in mormyromast regions of mormyrid electrosensory lobe. II. Cell types and corollary discharge plasticity

1992 ◽  
Vol 68 (3) ◽  
pp. 859-875 ◽  
Author(s):  
C. C. Bell ◽  
K. Grant
Keyword(s):  
Spontaneous Activity ◽  
Electric Organ Discharge ◽  
Single Cells ◽  
Receptive Fields ◽  
Electric Organ ◽  
Motor Command ◽  
Cell Types ◽  
Corollary Discharge ◽  
Sensory Stimuli ◽  
I Cells

1. This is the second of a series of papers on the electrosensory lobe and closely associated structures in electric fish of the family Mormyridae. The focus of the study is on the regions of the electrosensory lobe where primary afferent fibers from mormyromast electroreceptors terminate. 2. This second paper examines the responses of single cells in the mormyromast regions of the electrosensory lobe to electrosensory stimuli and to corollary discharge signals associated with the motor command that drives the electric organ to discharge. All recordings were extracellular. 3. Two major types of cells were identified: I cells, which were inhibited by electrosensory stimuli in the center of their receptive fields; and E cells, which were excited by such stimuli. 4. I cells and E cells shared a number of common features. Both types could have small receptive fields limited to only a few electroreceptors (3–5), and both types were markedly affected by the corollary discharge of the electric organ discharge (EOD) motor command. Cells of both types also showed clear plasticity in their responses to the corollary discharge or to the corollary discharge plus a stimulus. 5. I cells could be subdivided into three subtypes, I1, I2, and I3, on the basis of corollary discharge responses in the absence of sensory stimuli. I1 and I2 cells showed consistent corollary discharge bursts with little or no additional activity beyond the duration of the burst. The corollary discharge bursts of I1 cells were more stereotyped and of shorter latency than those of I2 cells. I3 cells had more spontaneous activity than I1 or I2 cells and minimal cells had more spontaneous activity than I1 or I2 cells and minimal corollary discharge responses in the absence of sensory stimuli. Field potentials indicated that all three subtypes of I cells were recorded in or near the ganglion layer of the electrosensory lobe. 6. Corollary discharge responses were plastic and depended on recent pairing of a sensory stimulus with the EOD motor command. Such plasticity was clearer in I2 and I3 cells than in I1 cells. Inhibitory sensory stimuli were paired with the EOD motor command for periods of a few seconds to several minutes. Such pairing resulted in a marked enhancement of the corollary discharge response in I2 cells, as shown by examining the effect of the motor command after turning off the stimulus. In I3 cells, such pairing resulted in a clear corollary burst to the command at the time of the previously paired inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Categorisation of Interpulse Intervals and Stochastic Analysis of Discharge Patterns in Resting Weak-Electric Mormyrid Fish (Gnathonemus Petersii)

Behaviour ◽  
1987 ◽  
Vol 102 (3-4) ◽  
pp. 264-282 ◽  
Author(s):  
Claudine TEYSSÈDRE ◽  
Michel Boudinot ◽  
Catherine Minisclou
Keyword(s):  
Individual Differences ◽  
Stochastic Analysis ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Electric Pulses ◽  
Oscillating Systems ◽  
Mormyrid Fish ◽  
Discharge Patterns ◽  
Gnathonemus Petersii ◽  
Criterion Method

AbstractInter-individual similarities in the electric organ discharge activity of immobile, isolated and undisturbed mormyrid fish were investigated. Two types of analysis were performed on the discharge patterns of 10 Gnathonemus petersii: (1) The Bout Interval Criterion method was used to categorise the intervals between consecutive electric pulses; (2) an analysis of sequences of acts was performed to study the serial ordering of the interpulse intervals. Interpulse intervals were demonstrated to belong to distinct classes, having similar limits for most animals. Most fish show five classes of interpulse intervals (23 to 68 ms; 69 to 108 ms; 109 to 170 ms; 171 to 212 ms; >212 ms), to which a sixth class (<23 ms) is added in some cases. Each class contains a similar number of intervals in all individuals. Particular associations were found between the occurrences of interpulse intervals belonging to different classes. Some of these associations (for example BB and EC) are displayed by most fish, whereas others express individual differences in the patterns of discharge. The discharge of immobile, undisturbed, isolated mormyrid fish is thus shown to present many similarities among individuals. Inter-individual differences exist only in the serial ordering of the intervals, where they arc best regarded as variations around a same theme. The absence of overlapping between the two main categories of interpulse intervals (category I: 69 to 108 ms; category II: 171 to 212 ms), as well as the constancy of their baselines, suggest that two oscillating systems participate to the electromotor command. The stochastic analysis of the serial ordering of the interpulse intervals suggest in addition that these two oscillators do not function independently. Momentaneous modifications of the activity of these two oscillators would provide an economical explanation for the various changes in the types of interpulse intervals associated with behavioural state or social interactions.

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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