Enhanced sensory sampling precedes self-initiated locomotion in an electric fish (original) (raw)
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Journal of Experimental Biology, 2014
How the brain processes natural sensory input remains an important and poorly understood problem in neuroscience. The efficient coding hypothesis asserts that the brain's coding strategies are adapted to the statistics of natural stimuli in order to efficiently process them, thereby optimizing their perception by the organism. Here we examined whether gymnotiform weakly electric fish displayed behavioral responses that are adapted to the statistics of the natural electrosensory envelopes. Previous studies have shown that the envelopes resulting from movement tend to consist of low (<1 Hz) temporal frequencies and are behaviorally relevant whereas those resulting from social interactions consist of higher (>1 Hz) temporal frequencies that can thus mask more behaviorally relevant signals. We found that the self-generated electric organ discharge frequency follows the detailed time course of the envelope around a mean value that is positively offset with respect to its baseline value for temporal frequencies between 0.001 Hz and 1 Hz. The frequency-following component of this behavioral response decreased in magnitude as a power law as a function of the envelope frequency and was negligible for envelope frequencies above 1 Hz. In contrast, the offset component was relatively constant and somewhat increased for envelope frequencies above 1 Hz. Thus, our results show that weakly electric fish display behavioral responses that track the detailed time course of low but not high frequency envelope stimuli. Furthermore, we found that the magnitude of the frequency-following behavioral response matches, in a one-to-one fashion, the spectral power of natural second-order stimulus attributes observed during movement. Indeed, both decayed as a power law with the same exponent for temporal frequencies spanning three orders of magnitude. Thus, our findings suggest that the neural coding strategies used by weakly electric fish perceive the detailed time course of movement envelopes and are adapted to their statistics as found in the natural environment. They also suggest that weakly electric fish might take advantage of the differential frequency content of movement and social envelopes in order to give appropriate behavioral responses during encounters between two or more conspecifics.
Neural Substrate of an Increase in Sensory Sampling Triggered by a Motor Command in a Gymnotid Fish
Journal of Neurophysiology, 2010
Despite recent advances that have elucidated the effects of collateral of motor commands on sensory processing structures, the neural mechanisms underlying the modulation of active sensory systems by internal motor-derived signals remains poorly understood. This study deals with the neural basis of the modulation of the motor component of an active sensory system triggered by a central motor command in a gymnotid fish. In Gymnotus omarorum, activation of Mauthner cells, a pair of reticulospinal neurons responsible for the initiation of escape responses in most teleosts, evokes an abrupt and prolonged increase in the rate of the electric organ discharge (EOD), the output signal of the electrogenic component of the active electrosensory system. We show here that prepacemaker neural structures (PPs) that control the discharge of the command nucleus for EODs are key elements of this modulation. Retrograde labeling combined with injections of glutamate at structures that contain labeled ...
Weakly electric fish are unique model systems in neuroethology, that allow experimentalists to non-invasively, access, central nervous system generated spatio-temporal electric patterns of pulses with roles in at least 2 complex and incompletely understood abilities: electrocommunication and electrolocation. Pulse-type electric fish alter their inter pulse intervals (IPIs) according to different behavioral contexts as aggression, hiding and mating. Nevertheless, only a few behavioral studies comparing the influence of different stimuli IPIs in the fish electric response have been conducted. We developed an apparatus that allows real time automatic realistic stimulation and simultaneous recording of electric pulses in freely moving Gymnotus carapo for several days. We detected and recorded pulse timestamps independently of the fish's position for days. A stimulus fish was mimicked by a dipole electrode that reproduced the voltage time series of real conspecific according to previously recorded timestamp sequences. We characterized fish behavior and the eletrocommunication in 2 conditions: stimulated by IPIs pre-recorded from other fish and random IPI ones. All stimuli pulses had the exact Gymontus carapo waveform. All fish presented a surprisingly long transient exploratory behavior (more than 8 h) when exposed to a new environment in the absence of electrical stimuli. Further, we also show that fish are able to discriminate between real and random stimuli distributions by changing several characteristics of their IPI distribution. Figure 10. Normalized Post Stimulus Time Histograms (PSTH).
Multimodal sensory integration in weakly electric fish: a behavioral account
Journal of Physiology-Paris, 2002
The ability to integrate multisensory information is a fundamental characteristic of the brain serving to enhance the detection and identification of external stimuli. Weakly electric fish employ multiple senses in their interactions with one another and with their inanimate environment (electric, visual, acoustic, mechanical, chemical, thermal, and hydrostatic pressure) and also generate signals using some of the same stimulus energies (electric, acoustic, visual, mechanical). A brief overview provides background on the sensory and motor channels available to the fish followed by an examination of how weakly electric fish 'benefit' from integrating various stimulus modalities that assist in prey detection, schooling, foraging, courtship, and object location. Depending on environmental conditions, multiple sensory inputs can act synergistically and improve the task at hand, can be redundant or contradictory, and can substitute for one another. Over time, in repeated encounters with familiar surrounds, loss of one modality can be compensated for through learning. Studies of neuronal substrates and an understanding of the computational algorithms that underlie multisensory integration ought to expose the physiological corollaries to widely published concepts such as internal representation, sensory expectation, sensory generalization, and sensory transfer.
Experimental Results, 2020
Evaluation of neural activity during natural behaviours is essential for understanding how the brain works. Here we show that neuron-specific self-evoked firing patterns are modulated by an object’s presence, at the electrosensory lobe neurons of tethered-moving Gymnotus omarorum. This novel preparation shows that electrosensory signals in these pulse-type weakly electric fish are not only encoded in the number of spikes per electric organ discharge (EOD), as is the case in wave-type electric fish, but also in the spike timing pattern after each EOD, as found in pulse-type Mormyroidea. Present data suggest that pulsant electrogenesis and spike timing coding of electrosensory signals developed concomitantly in the same species, and evolved convergently in African and American electric fish.
Behavioural Brain Research, 1984
In the presence of a novel stimulus such as an aluminum or a plastic rod mormyrid fish (Marcusenius cyprinoides and Gnathonemus petersii) exhibit characteristic motor probing acts (PMAs): 'chin probing', 'radial' and 'lateral va-et-vient', 'lateral probing', 'tangential probing', and 'stationary probing'. During the display of these PMAs the fish maintain characteristic probing distances from the object which were 4.5 cm for the metal and 2.5-3.7 cm for the plastic stimulus. G. petersii with their electric organ rendered inoperative ('silent fish') no longer exhibited 'radial' and 'lateral va-et-vient'. Regardless of the nature of the stimulus the probing distances were shorter in 'silent' fish and ranged from 1.8 to 2.6 cm. During the display of PMAs intact fish changed their variable electric organ discharge rate to a unique and stable, regularized rate, with the interdischarge interval maintained at 28-30 ms. The fish's electric and non-electric (motor) probing behavior in the presence of novel objects (and following their removal during phantom PMAs) is discussed in light of theories on exploratory behavior..
The neuronal correlate of locomotion in fish
Experimental Brain Research, 1980
An in vitro preparation of the lamprey spinal cord was developed to enable detailed studies of the neuronal organization of the central spinal network generating fish swimming movements, one basic type of vertebrate locomotion. 1. In the isolated lamprey spinal cord, stable bursting activity recorded in the ventral roots was initiated by adding, e.g., Dglutamate or L-DOPA to the bathing solution. Less stable rhythmic activity could also be induced by tonic electrical stimulation of the spinal cord. 2. The isolated spinal cord is capable of producing rhythmic activity with the same type of intra-and intersegmental coordination as in the swimming fish, i.e., with alternation between the two sides of the segment and an intersegmental phase coupling. Hence, the in vitro preparation of the lamprey spinal cord may be said to represent the neuronal correlate of the undulatory swimming movements of fish. 3. By performing spinal cord transections it was demonstrated that as few as four segments can produce rhythmic activity with maintained coordination. It was concluded that the capacity to produce coordinated burst activity is distributed throughout the lamprey spinal cord. 4. A longitudinal midline lesion as long as four segments did not prevent the ventral roots on each side from bursting with maintained coordination between adjacent hemisegments. Thus, one side of a segment can produce bursting without interaction with its opposite side, at least when connected to its rostral and caudal neighbors. 5. The rate of bursting was found to vary from one cycle to the next with the period * This work was supported by the Swedish Medical Research Council (14X-3026) and by the Karolinska Institute. A.H.