Kirsty Grant

Electric fish measure distance in the dark

Distance determination in animals can be achieved by visual or non-visual cues. Weakly electric fish use active electrolocation for orientation in the dark. By perceiving self-produced electric signals with epidermal electroreceptors, fish can detect, locate and analyse nearby objects. Distance discrimination, however, was thought to be hardly possible because it was assumed that confusing ambiguity could arise with objects of unknown sizes and materials. Here we show that during electrolocation electric fish can measure the distance of most objects accurately, independently of size, shape and material. Measurements of the ‘electric image’ projected onto the skin surface during electrolocation revealed only one parameter combination that was unambiguously related to object distance: the ratio between maximal image slope and maximal image amplitude. However, slope-to-amplitude ratios for spheres were always smaller than those for other objects. As predicted, these objects were erroneously judged by the fish to be further away than all other objects at an identical distance. Our results suggest a novel mechanism for depth perception that can be achieved with a single, stationary two-dimensional array of detectors.

Reversible Associative Depression and Nonassociative Potentiation at a Parallel Fiber Synapse

The electrosensory lobe (ELL) of mormyrid electric fish is one of several cerebellum-like sensory structures in fish that remove predictable features of the sensory inflow. This adaptive process obeys anti-Hebbian rules and appears to be mediated by associative depression at the synapses between parallel fibers and Purkinje-like cells of ELL. We show here that there is also a nonassociative potentiation at this synapse that depends only on the repeated occurrence of the EPSP. The depression can be reversed by the potentiation and vice versa. Finally, we show that the associative depression requires NMDA receptor activation, changes in postsynaptic calcium, and the occurrence of a postsynaptic dendritic spike within a few milliseconds following EPSP onset.

Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation.

SUMMARY Weakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation, nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance, can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response (novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions – the Schnauzenorgan and the nasal region – can be termed electric fovea but they serve separate functions during active electrolocation.

The Mormyrid Electrosensory Lobe In Vitro: Physiology and Pharmacology of Cells and Circuits

This paper is concerned with the electrosensory lobe (ELL) of mormyrid electric fish as examined in in vitro slices. Intracellular recordings from morphologically identified cells and field potential recordings were used to characterize the physiology and pharmacology of ELL cells. Most intracellular recordings were from the Purkinje-like interneurons that are known as medium ganglion cells and from the two types of efferent neurons, large ganglion and large fusiform cells. Stimulation of primary afferent fibers elicits both excitatory and inhibitory effects in these cells, with the excitatory effects being mediated by both the AMPA and NMDA types of glutamate receptors and the inhibitory effects being mediated by both GABAA and glycine receptors. Parallel-fiber stimulation evokes an EPSP–IPSP sequence, with the EPSPs being mediated by both AMPA and NMDA receptors and the IPSPs being mediated by GABAA receptors only. The parallel fiber-evoked EPSPs and IPSPs show marked paired-pulse facilitation. A large and unusually broad spike is recorded inside medium ganglion cells, and field potential responses suggest that this spike is propagated into the apical dendrites. The results provide essential information for understanding how peripheral and central inputs are integrated in ELL.

Interneurons of the ganglionic layer in the mormyrid electrosensory lateral line lobe: Morphology, immunohistochemistry, and synaptology

This is the second paper in a series that describes the morphology, immunohistochemistry, and synaptology of the mormyrid electrosensory lateral line lobe (ELL). The ELL is a highly laminated cerebellum‐like structure in the rhombencephalon that subserves an active electric sense: Objects in the nearby environment of the fish are detected on the basis of changes in the reafferent electrosensory signals that are generated by the animals own electric organ discharge. The present paper describes interneurons in the superficial (molecular, ganglionic, and plexiform) layers of the ELL cortex that were analyzed in the light and electron microscopes after Golgi impregnation, intracellular labeling, neuroanatomical tracing, and γ‐aminobutyric acid (GABA) immunohistochemistry.

Functional Foveae in an Electrosensory System

Several species of Mormyrid weakly electric fish have a mobile chin protuberance that serves as a mobile antenna during prey detection, tracking behaviors, and foraging for food. It has been proposed that it constitutes a fovea of the electrosensory system. The distribution of the three types of receptor organs involved in active imaging of the local surroundings, prey detection, and passive electroreception, and their central projection to the electrosensory lobe (ELL), have been studied in Gnathonemus petersii. Density distributions were compared for different body regions. Primary afferent projections were labeled with biocytin or biotinylated dextrans. This showed that there is considerable central “over‐representation” of the mandibular and nasal regions of the sensory surface involved in electrolocation, at the expense of the other body regions investigated. This over‐representation is not a mere effect of the very high density of receptor organs in these areas, but is found to be due to central magnification. This magnification differs between the subclasses of electroreceptors, suggesting a functional segregation in the brain. We conclude that the chin protuberance and the nasal region are the regions of greatest sensitivity for the resistive, capacitive, and low‐frequency characteristics of the environment, and are probably most important in prey detection, whereas other regions of the skin with a lesser resolution and sensitivity to phase distortion of the EOD, in particular the trunk, are probably designed for imaging larger, inanimate features of the environment. Our data support the hypothesis that the chin appendage and nasal region are functionally distinct electrosensory foveae. J. Comp. Neurol. 511:342–359, 2008.

Projection neurons of the mormyrid electrosensory lateral line lobe: Morphology immunohistochemistry, and synaptology

This paper describes the morphological, immunohistochemical, and synaptic properties of projection neurons in the highly laminated medial and dorsolateral zones of the mormyrid electrosensory lateral line lobe (ELL). These structures are involved in active electrolocation, i.e., the detection and localization of objects in the nearby environment of the fish on the basis of changes in the reafferent electrosensory signal generated by the animals own electric organ discharge. Electrosensory, corollary electromotor command‐associated signals (corollary discharges), and a variety of other inputs are integrated within the ELL microcircuit. The organization of ELL projection neurons is analyzed at the light and electron microscopic levels based on Golgi impregnations, intracellular labeling, neuroanatomical tracer techniques, and γ‐aminobutyric acid (GABA), γ‐aminobutyric acid decarboxylase (GAD), and glutamate immunohistochemistry.

Electric imaging through active electrolocation: implication for the analysis of complex scenes

The electric sense of mormyrids is often regarded as an adaptation to conditions unfavourable for vision and in these fish it has become the dominant sense for active orientation and communication tasks. With this sense, fish can detect and distinguish the electrical properties of the close environment, measure distance, perceive the 3-D shape of objects and discriminate objects according to distance or size and shape, irrespective of conductivity, thus showing a degree of abstraction regarding the interpretation of sensory stimuli. The physical properties of images projected on the sensory surface by the fish’s own discharge reveal a “Mexican hat” opposing centre-surround profile. It is likely that computation of the image amplitude to slope ratio is used to measure distance, while peak width and slope give measures of shape and contrast. Modelling has been used to explore how the images of multiple objects superimpose in a complex manner. While electric images are by nature distributed, or ‘blurred” behavioural strategies orienting sensory surfaces and the neural architecture of sensory processing networks both contribute to resolving potential ambiguities. Rostral amplification is produced by current funnelling in the head and chin appendage regions, where high density electroreceptor distributions constitute foveal regions. Central magnification of electroreceptive pathways from these regions particularly favours the detection of capacitive properties intrinsic to potential living prey. Swimming movements alter the amplitude and contrast of pre-receptor object-images but image modulation is normalised by central gain-control mechanisms that maintain excitatory and inhibitory balance, removing the contrast-ambiguity introduced by self-motion in much the same way that contrast gain-control is achieved in vision.

Myelinated dendrites in the mormyrid electrosensory lobe.

This is the third paper in a series on the morphology, immunohistochemistry, and synaptology of the mormyrid electrosensory lateral line lobe (ELL). The ELL is a highly laminated, cerebellum‐like structure in the rhombencephalon that subserves an active electric sense: Objects in the nearby environment are detected on the basis of changes in the reafferent electrosensory signals that are generated by the animals own electric organ discharge. This paper concentrates on the intermediate (cell and fiber) layer of the medial zone of the ELL and pays particular attention to the large multipolar neurons of this layer (LMI cells). LMI cells are γ‐aminobutyric acid (GABA)ergic and have one axon and three to seven proximal dendrites that all become myelinated after their last proximal branching point. The axon projects to the contralateral homotopic region and has ipsilateral collaterals. Both ipsilaterally and contralaterally, it terminates in the deep and superficial granular layers. The myelinated dendrites end in the deep granular layer, where they most likely do not make postsynaptic specializations, but do make presynaptic specializations, similar to those of the LMI axons. Because it is not possible to distinguish between axonal and dendritic LMI terminals in the granular layer, the authors refer to both as LMI terminals. These are densely filled with small, flattened vesicles and form large appositions with ELL granular cell somata and dendrites with symmetric synaptic membrane specializations. LMI cells do not receive direct electrosensory input on their somata, but electrophysiological recordings suggest that they nevertheless respond strongly to electrosensory signals (Bell [ 1990 ] J. Neurophysiol. 63:303–318). Consequently, the authors speculate that the myelinated dendrites of LMI cells are excited ephaptically (i.e., by electric field effects) by granular cells, which, in turn, are excited via mixed synapses by mormyromast primary afferents. The authors suggest that this ephaptic activation of the GABAergic presynaptic terminals of the myelinated dendrites may trigger immediate synaptic release of GABA and, thus, may provide a very fast local feedback inhibition of the excited granular cells in the center of the electrosensory receptive field. Subsequent propagation of the dendritic excitation down the myelinated dendrites to the somata and axon hillocks of LMI cells probably generates somatic action potentials, resulting in the spread of inhibition through axonal terminals to a wide region around the receptive field center and in the contralateral ELL. Similar presynaptic myelinated dendrites that subserve feedback inhibition, until now, have not been described elsewhere in the brain of vertebrates. J. Comp. Neurol. 431:255–275, 2001.

Mormyrid electrosensory lobe in vitro: morphology of cells and circuits.

The electrosensory lobe (ELL) of mormyrid electric fish is a cerebellum‐like brainstem structure that receives the primary afferent fibers from electroreceptors in the skin. The ELL and similar sensory structures in other fish receive extensive input from other central sources in addition to the peripheral input. The responses to some of these central inputs are adaptive and serve to minimize the effects of predictable sensory inputs. Understanding the interaction between peripheral and central inputs to the mormyrid ELL requires knowledge of its functional circuitry, and this paper examines this circuitry in the in vitro slice preparation and describes the axonal and dendritic morphology of major ELL cell types based on intracellular labeling with biocytin. The cells described include medium ganglion cells, large ganglion cells, large fusiform cells, thick‐smooth dendrite cells, small fusiform cells, granule cells, and primary afferent fibers. The medium ganglion cells are Purkinje‐like interneurons that terminate on the two types of efferent cells, i.e., large ganglion and large fusiform cells, as well as on each other. These medium ganglion cells fall into two morphologically distinct types based on the distributions of basal dendrites and axons. These distributions suggest hypotheses about the basic circuit of the ELL that have important functional consequences, such as enhancement of contrast between “on” elements that are excited by increased afferent activity and “off” elements that are inhibited. J. Comp. Neurol. 404:359–374, 1999.