Physiology of Tuberous Electrosensory Systems

Kawasaki, Masashi

doi:10.1007/0-387-28275-0_7

Cited by 39 publications

(33 citation statements)

References 170 publications

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“…Some researchers have challenged the existence of two categories of afferents (Viancour, 1979), but more recent work has clearly shown that P-and T-units give rise to functionally and anatomically distinct central pathways (Maler et al, 1981;Carr and Maler, 1986;Mathieson et al, 1987;Heiligenberg, 1991;Kawasaki, 2005). Indeed, our results reveal separate populations of amplitude-and time-coding afferents that agree with our a priori classification of P-and T-units, respectively (Fig.…”

Section: Discussionsupporting

confidence: 87%

“…Many neurons in the hindbrain and midbrain process information relevant to both the JAR and active electrolocation (Bell and Maler, 2005;Kawasaki, 2005). In fact, jamming of electrolocation occurs in the presence of a neighbor with a similar EOD frequency because the resulting interference induces AM and PM within the same frequency range that is relevant for detecting objects passing through the electric field (Heiligenberg, 1973).…”

Section: Discussionmentioning

confidence: 99%

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Ambiguous Encoding of Stimuli by Primary Sensory Afferents Causes a Lack of Independence in the Perception of Multiple Stimulus Attributes

Carlson¹,

Kawasaki²

2006

J. Neurosci.

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Accurate sensory perception often depends on the independent encoding and subsequent integration of multiple stimulus attributes. In the weakly electric fish Eigenmannia, P-and T-type primary afferent fibers are specialized for encoding the amplitude and phase, respectively, of electrosensory stimuli. We used a stimulus estimation technique to quantify the ability of P-and T-units to encode random modulations in amplitude and phase. As expected, P-units exhibited a clear preference for encoding amplitude modulations, whereas T-units exhibited a clear preference for encoding phase modulations. Surprisingly, both types of afferents also encoded their nonpreferred stimulus attribute when it was presented in isolation or when the preferred stimulus attribute was sufficiently weak. Because afferent activity can be affected by modulations in either amplitude or phase, it is not possible to unambiguously distinguish between these two stimulus attributes by observing the activity of a single afferent fiber. Simple model neurons with a preference for encoding either amplitude or phase also encoded their nonpreferred stimulus attribute when it was presented in isolation, suggesting that such ambiguity is unavoidable. Using the well known jamming avoidance response as a probe of electrosensory perception, we show that the ambiguity at the single-neuron level gives rise to a systematic misrepresentation of stimuli at the population level and a resulting misperception of the amplitude and phase of electrosensory stimuli.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Ambiguous Encoding of Stimuli by Primary Sensory Afferents Causes a Lack of Independence in the Perception of Multiple Stimulus Attributes

Carlson¹,

Kawasaki²

2006

J. Neurosci.

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“…Neurons with similar characteristics and functional significance are present in the electrosensory systems of wave gymnotids (Szabo et al, 1975;Heiligenberg, 1991;Mehaffey et al, 2006), pulse (Bell and Grant, 1989;XuFriedman and Hopkins, 1999) and wave (Kawasaki, 2005) mormyrids, as well as in the auditory (Carr et al, 2005) and somatosensory (Prescott and De Koninck, 2002) systems of higher vertebrates.…”

Section: Comparative Considerations About Single Spiking Cellsmentioning

confidence: 99%

The role of single spiking spherical neurons in a fast sensory pathway

Nogueira

Castelló

Caputi

2006

Journal of Experimental Biology

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SUMMARY One difficulty in understanding the brain is that of linking the structure of the neurons with their computational roles in neural circuits. In this paper we address this subject in a relative simple system, the fast electrosensory pathway of an electric fish, where sensory images are coded by the relative latency of a volley of single spikes. The main input to this path is a stream of discrete electric images resulting from the modulation of a self-generated carrier by the environment. At the second order cell level, a window of low responsiveness, reducing potential interference from other stimuli, follows activation of the path. In the present study, we further characterize the input–output relationship at the second order neurons by recording field potentials, and ascertain its cellular basis using in vitro whole cell patch recordings. The field potentials from freely behaving, socially interacting fish were obtained from chronically implanted fish restrained in a mesh pen. In addition, at the end of some experiments the fish was curarized and the fast electrosensory path responses to artificial stimuli were further explored. These in vivo approaches showed that larger stimuli cause larger and longer windows of low responsiveness. The simple spherical geometry of the second order cells allowed us to unveil the membrane mechanisms underlying this phenomenon in vitro. These spherical cells respond with a single spike at the onset of current steps of any amplitude and duration, showing inward and outward rectification, and a long refractory period. We postulate that a low-threshold K+ conductance generates the outward rectification. The most parsimonious interpretation of our data indicates that slow deactivation of this conductance causes the long refractory period. These non-linear properties of the membrane explain the single spiking profile of spherical cells and the low-responsiveness window observed in vivo. Since the electric organ discharges are emitted at intervals slightly longer than the duration of the low-responsiveness window,we propose that the described cellular mechanisms allow fish streaming self-generated images.

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“…The resulting changes in the transcutaneous electric field are transduced by cutaneous electroreceptors and encoded as train of spikes in primary electroreceptive afferents (Bullock et al, 1961;Fessard and Szabo, 1961;Lissmann, 1958;Szabo and Fessard, 1974;Wright, 1958). This information is further processed in the brain stem (Aumentado-Armstrong et al, 2015;Bell and Maler, 2005;Heiligenberg and Rose, 1985;Kawasaki, 2005) and telencephalon (Harvey Girard et al, 2010;Trinh et al, 2016), giving origin to reflex Post and von der Emde, 1999), stereotyped (Heiligenberg, 1991;Kawasaki, 2005;Moller, 1995) and learned behaviors (Jun et al, 2014;Schumacher et al, 2016;Walton and Moller, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…While T and S units fire a single spike phase locked with many but not all zero crossing of the sLEOD (Heiligenberg, 1991), P and O units are characterized by a probability of firing proportional to the amplitude of the local signal (Benda et al, 2005(Benda et al, , 2006Chacron et al, 2000Chacron et al, , 2005Kawasaki, 2005).…”

Section: Introductionmentioning

confidence: 99%

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

Rodríguez-Cattáneo

Aguilera

Caputi

2017

Journal of Experimental Biology

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As in most sensory systems, electrosensory images in weakly electric fish are encoded in two parallel pathways, fast and slow. From work on wave-type electric fish, these fast and slow pathways are thought to encode the time and amplitude of electrosensory signals, respectively. The present study focuses on the primary afferents giving origin to the slow path of the pulse-type weakly electric fish Gymnotus omarorum. We found that burst duration coders respond with a high-frequency train of spikes to each electric organ discharge. They also show high sensitivity to phase-frequency distortions of the self-generated local electric field. We explored this sensitivity by manipulating the longitudinal impedance of a probe cylinder to modulate the stimulus waveform, while extracellularly recording isolated primary afferents. Resistive loads only affect the amplitude of the re-afferent signals without distorting the waveform. Capacitive loads cause large waveform distortions aside from amplitude changes. Stepping from a resistive to a capacitive load in such a way that the stimulus waveform was distorted, without changing its total energy, caused strong changes in latency, inter-spike interval and number of spikes of primary afferent responses. These burst parameters are well correlated suggesting that they may contribute synergistically in driving downstream neurons. This correlation also suggests that each receptor encodes a single parameter in the stimulus waveform. The finding of waveform distortion sensitivity is relevant because it may contribute to: (a) enhance electroreceptive range in the peripheral 'electrosensory field', (b) a better identification of living prey at the 'foveal electrosensory field' and (c) detect the presence and orientation of conspecifics. Our results also suggest a revision of the classical view of amplitude and time encoding by fast and slow pathways in pulse-type electric fish.

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Physiology of Tuberous Electrosensory Systems

Cited by 39 publications

References 170 publications

Ambiguous Encoding of Stimuli by Primary Sensory Afferents Causes a Lack of Independence in the Perception of Multiple Stimulus Attributes

Ambiguous Encoding of Stimuli by Primary Sensory Afferents Causes a Lack of Independence in the Perception of Multiple Stimulus Attributes

The role of single spiking spherical neurons in a fast sensory pathway

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

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