Physiological evidence of sensory integration in the electrosensory lateral line lobe of Gnathonemus petersii (original) (raw)
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The cellular and circuit basis for evolutionary change in sensory perception in mormyrid fishes
Scientific reports, 2017
Species differences in perception have been linked to divergence in gross neuroanatomical features of sensory pathways. The anatomical and physiological basis of evolutionary change in sensory processing at cellular and circuit levels, however, is poorly understood. Here, we show how specific changes to a sensory microcircuit are associated with the evolution of a novel perceptual ability. In mormyrid fishes, the ability to detect variation in electric communication signals is correlated with an enlargement of the midbrain exterolateral nucleus (EL), and a differentiation into separate anterior (ELa) and posterior (ELp) regions. We show that the same cell types and connectivity are found in both EL and ELa/ELp. The evolution of ELa/ELp, and the concomitant ability to detect signal variation, is associated with a lengthening of incoming hindbrain axons to form delay lines, allowing for fine temporal analysis of signals. The enlargement of this brain region is also likely due to an ov...
Journal of Experimental Biology, 2008
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.
Sensory processing in the pallium of a mormyrid fish
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1998
To investigate the functional organization of higher brain levels in fish we test the hypothesis that the dorsal gray mantle of the telencephalon of a mormyrid fish has discrete receptive areas for several sensory modalities. Multiunit and compound field potentials evoked by auditory, visual, electrosensory, and water displacement stimuli in this weakly electric fish are recorded with multiple semimicroelectrodes placed in many tracks and depths in or near telencephalic area dorsalis pars medialis (Dm). Most responsive loci are unimodal; some respond to two or more modalities. Each modality dominates a circumscribed area, chiefly separate. Auditory and electrical responses cluster in the dorsal 500 micrometer of rostral and caudolateral Dm, respectively. Two auditory subdivisions underline specialization of this sense. Mechanoreception occupies a caudal area overlapping electroreception but centered 500 micrometer deeper. Visual responses scatter widely through ventral areas. Audito...
Frontiers in Behavioral Neuroscience, 2012
This study examined the contributions of passive and active membrane properties to the temporal selectivities of electrosensory neurons in vivo. The intracellular responses to timevarying (2-30 Hz) electrosensory stimulation and current injection of 27 neurons in the midbrain of the weakly electric fish Eigenmannia were recorded. Each neuron was filled with biocytin to reveal its anatomy. Neurons were divided into two biophysically distinct groups based on their frequency-dependent responses to sinusoidal current injection over the range 2-30 Hz. Fourteen neurons showed low-pass filtering, with a maximum decline in the amplitude of voltage responses of Ͼ2.6 dB (X ϭ 4.30 dB, s ϭ 1.10 dB) to sinusoidal current injection. These neurons also showed low-pass filtering of electrosensory information but with larger maximum declines in postsynaptic potential amplitude (X ϭ 9.53 dB, s ϭ 3.34 dB; n ϭ 10). These neurons had broad dendritic arbors and relatively spiny dendrites. Five neurons showed all-pass filtering, having maximum decline in the amplitude of voltage responses of Ͻ2.0 dB (X ϭ 1.16 dB, s ϭ 0.61 dB). For electrosensory stimuli, however, these neurons showed low-, band-, or high-pass filtering. These neurons had small dendritic arbors and few or no spines. Voltage-dependent "active" conductances were revealed in eight neurons by using several levels of current clamp. In four of these neurons, the duration of the voltage-dependent conductances decreased in concert with the period of the electrosensory stimulus, whereas in the other four neurons the duration of the voltage-dependent conductances was relatively short (Ͻ30 msec) and nearly constant across sensory stimulation frequencies. These conductances enhanced the temporal filtering properties of neurons.
Physiology and Plasticity of Morphologically Identified Cells in the Mormyrid Electrosensory Lobe
The Journal of Neuroscience, 1997
The electrosensory lobe (ELL) of mormyrid electric fish is the first stage in the central processing of sensory input from electroreceptors. The responses of cells in ELL to electrosensory input are strongly affected by corollary discharge signals associated with the motor command that drives the electric organ discharge (EOD). This study used intracellular recording and staining to describe the physiology of three major cell types in the mormyrid ELL: the medium ganglion cell, the large ganglion cell, and the large fusiform cell. The medium ganglion cell is a Purkinje-like interneuron, whereas the large ganglion and large fusiform cells are efferent neurons that convey electrosensory information to higher stages of the system. Clear differences were observed among the three cell types. Medium ganglion cells showed two types of spikes, a small narrow spike and a large broad spike that were probably of axonal and dendro-somatic origin, respectively, whereas the large ganglion and large fusiform cells showed only large narrow spikes. Most of the medium ganglion cells and all of the large ganglion cells were inhibited by electrosensory stimuli in the center of their receptive fields, whereas the large fusiform cells were excited by such stimuli. Responses to the EOD corollary discharge were different in the three cell types, and these responses underwent plastic changes after a few minutes of pairing with an electrosensory stimulus. Plastic changes were also observed in medium and large ganglion cells after the corollary discharge was paired with depolarizing, intracellular current pulses.
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 1997
Modi®cation of an existing neural structure to support a second function will produce a trade-o between the two functions if they are in some way incompatible. The trade-o between two such sensory functions is modeled here in pyramidal neurons of the gymnotiform electric ®sh's medullar electrosensory lateral line lobe (ELL). These neurons detect two electric stimulus features produced when a nearby object interferes with the ®sh's autogenous electric ®eld: (1) amplitude modulation across a cell's entire receptive ®eld and (2) amplitude variation within a cell's receptive ®eld 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-o and that the severity of the tradeo depends on the particular algorithm of sensory integration. Electrophysiology data indicate that of the two algorithms for sensory integration modeled here for the gymnotiform ®sh Brachyhypopomus pinnicaudatus, the algorithm with the better trade-o function is used. Further, the intrinsic trade-o within single cells has been surmounted by the replication of ELL into multiple electrosensory map segments, each specialized to emphasize dierent sensory features.
eLife, 2016
Recently, we reported evidence for a novel mechanism of peripheral sensory coding based on oscillatory synchrony. Spontaneously oscillating electroreceptors in weakly electric fish (Mormyridae) respond to electrosensory stimuli with a phase reset that results in transient synchrony across the receptor population (Baker et al., 2015). Here, we asked whether the central electrosensory system actually detects the occurrence of synchronous oscillations among receptors. We found that electrosensory stimulation elicited evoked potentials in the midbrain exterolateral nucleus at a short latency following receptor synchronization. Frequency tuning in the midbrain resembled peripheral frequency tuning, which matches the intrinsic oscillation frequencies of the receptors. These frequencies are lower than those in individual conspecific signals, and instead match those found in collective signals produced by groups of conspecifics. Our results provide further support for a novel mechanism for ...