Responses of electrosensory neurons in the torus semicircularis of Eigenmannia to complex beat stimuli: testing hypotheses of temporal filtering

Rose, Garrett S.; Etter, Nicole M.; Alder, Todd B.

doi:10.1007/bf00199254

Cited by 8 publications

(4 citation statements)

References 32 publications

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“…EOD frequency differences between fish are detected as direct inputs to the ELL. At very high EOD frequency differences (Ͼ200 Hz), the P units and thus the pyramidal cells can no longer reliably track the stimulus (unpublished data); furthermore, midbrain neurons in receipt of ELL input respond mostly to lower frequencies in a related wave-type gymnotiform fish (40).…”

Section: Discussionmentioning

confidence: 99%

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Middleton

Longtin²,

Benda³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

100

115

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Sensory stimuli often have rich temporal and spatial structure. One class of stimuli that are common to visual and auditory systems and, as we show, the electrosensory system are signals that contain power in a narrow range of temporal (or spatial) frequencies. Characteristic of this class of signals is a slower variation in their amplitude, otherwise known as an envelope. There is evidence suggesting that, in the visual cortex, both narrowband stimuli and their envelopes are coded for in separate and parallel streams. The implementation of this parallel transmission is not well understood at the cellular level. We have identified the cellular basis for the parallel transmission of signal and envelope in the electrosensory system: a two-cell network consisting of an interneuron connected to a pyramidal cell by means of a slow synapse. This circuit could, in principle, be implemented in the auditory or visual cortex by the previously identified biophysics of cortical interneurons.parallel processing ͉ sensory systems ͉ stimulus envelopes N arrowband signals (i.e., containing power in a narrow range of frequencies) are an important class of naturalistic stimuli for visual and auditory systems and have associated with them a stimulus envelope, a slow, time-varying contrast or modulation of a sinusoidal carrier arising naturally from, for example, interference between two or more sinusoidal oscillations with similar frequencies. Amplitude-modulated signals have no power at the frequencies of the modulation; instead, they have power centered on the carrier frequency with side bands whose structure depends on the frequency content of the modulation or envelope (1). Because the actual signal contains no power at the envelope frequencies, a system that can extract information about the envelope must use nonlinear processing. An asymmetry in the single-neuron inputoutput transfer, such as rectification (1), will generate power at the envelope frequencies (2, 3). Recent studies show that visual cortical neurons in cats respond to both low spatial frequency signals and the low-frequency spatial envelopes of high-frequency signals and also suggest that information about stimuli and their envelopes take separate and mutually exclusive linear and nonlinear pathways to reach these cortical neurons (4-11). The cellular and network basis of these parallel cortical computations is not, however, understood.Apteronotus leptorhynchus generates a sinusoidal electric organ discharge (EOD) that produces an electric field around its body. Recent field studies have shown that A. leptorhynchus and related species forage in groups (12) (E. W. Tan and E. S. Fortune, personal communication). Although individual A. leptorhynchus maintain a stable EOD frequency (13), the species has a frequency range of Ϸ700-1,000 Hz. Two fish with widely spaced EOD frequencies will generate a high-frequency envelope of their EOD that is referred to as an amplitude modulation (AM) or beat. Additional fish can superimpose a slowly varying contrast on this high-...

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Section: Discussionmentioning

confidence: 99%

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Middleton

Longtin²,

Benda³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

100

115

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“…An important question, therefore, is whether processes for PSP depression impede responses to slow changes in signal amplitude that are concurrent with or directly follow fast AMs. Rose et al (1994) showed that superimposing fast modulations onto slow modulations did not attenuate the slow PSPs of lowpass toral neurons. Because PSP depression was not measured in that study, the findings suggest, but do not prove, that PSP depression does not preclude response to low-temporal frequency information.…”

Section: Behavioral Considerationsmentioning

confidence: 99%

Frequency-Dependent PSP Depression Contributes to Low-Pass Temporal Filtering inEigenmannia

Rose

Fortune

1999

J. Neurosci.

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This study examined the contribution of frequency-dependent short-term depression of PSP amplitude to low-pass temporal filtering in the weakly electric fish Eigenmannia. Behavioral and neurophysiological methods were used. Decelerations of the electric organ discharge frequency were measured in response to continuous and discontinuous electrosensory stimuli. Decelerations were strongest (median ϭ 4.7 Hz; range, 3.5-5.9 Hz) at continuous beat rates of ϳ5 Hz and weakest (median ϭ 0.4 Hz; range, 0.0-0.8 Hz) at beat rates of 30 Hz. Gating 20 or 30 Hz stimuli at a rate of 5 Hz, however, elicited decelerations that were sixfold greater than that of continuous stimuli at these beat rates (median ϭ 2.6 Hz; range, 2.0-4.7 Hz for 30 Hz). These results support the hypothesis that short-term processes enhance low-pass filtering by reducing responses to fast beat rates. This hypothesis was tested by recording intracellularly the responses of 33 midbrain neurons to continuous and discontinuous stimuli. Results indicate that short-term depression of PSP amplitude primarily accounts for the steady-state lowpass filtering of these neurons beyond that contributed by their passive and active membrane properties. Previous results demonstrate that passive properties can contribute up to 7 dB of low-pass filtering; PSP depression can add up to an additional 12.5 dB (median ϭ 4.5). PSP depression increased in magnitude with stimulus frequency and showed a prominent short-term component (t 1 ϭ 66 msec at 30 Hz). Initial PSP amplitude recovered fully after a gap of 150 msec for most neurons. Remarkably, recovery of PSP amplitude could be produced by inserting a brief low-temporal frequency component in the stimulus.

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“…These factors help account for the finding that superimposing a fast beat pattern (amplitude modulation) on a slower pattern generally failed to diminish a neuron's response to the slower component (Rose et al, 1994).…”

Section: Network Processesmentioning

confidence: 99%

Short-Term Synaptic Plasticity Contributes to the Temporal Filtering of Electrosensory Information

2000

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Short-term synaptic depression and facilitation often are elicited by different temporal patterns of activity. Short-term plasticity may contribute, therefore, to temporal filtering by impeding synaptic transmission for some temporal patterns of activity and facilitating transmission for other patterns. We examined this hypothesis by investigating whether short-term plasticity contributes to the temporal filtering properties of midbrain electrosensory neurons. Postsynaptic potentials were recorded in response to sensory stimuli and to direct stimulation of afferents, in vivo. Stimulating afferents with pairs of pulses at a rate of 20 pairs/sec ["tetanus (20 Hz)"] induced PSP depression. This PSP depression was similar to that observed for electrosensory stimuli of the same temporal frequency. Analysis of PSPs elicited by a pair of pulses that preceded versus followed the tetanus revealed that PSP depression was caused by synaptic depression, not by a loss of facilitation. Behavioral studies indicate that fish can detect slow changes in signal amplitude (slow AM) in backgrounds of fast fluctuations. Correspondingly, midbrain neurons respond well to slow AM even in the presence of fast AM. In many neurons, facilitation enhanced responses to trains (8-10 pulses; 100 Hz) that represented activity patterns elicited by slow AM, despite induction of synaptic depression by a tetanus (20 Hz). The interplay between synaptic depression and facilitation, therefore, can act as a filter of temporal information. Some neurons that showed little facilitation nonetheless responded to low temporal-frequency information after induction of depression by fast information; this likely results from the convergence of inputs with different temporal filtering properties.Key words: whole-cell patch; sensory processing; synaptic depression; facilitation; jamming avoidance response; in vivo; midbrain; intracellular Synaptic plasticity is an increase or decrease in the efficacy of synaptic transmission with use. Increases or decreases in efficacy that occur over tens of milliseconds are referred to as facilitation and short-term depression, respectively (Zucker, 1989(Zucker, , 1999.Although short-term synaptic plasticity appears to be widespread in nervous systems and across taxa, comparatively little is known concerning its function in neural circuits and behavior. Depression can be linked to habituation of the gill withdrawal reflex in Aplysia (Castellucci and Kandel, 1974) and escape-related reflexes in fish, crayfish, and insects. Facilitation has been related to the dishabituation of reflexes of this type. The ubiquity of short-term plasticity in other types of circuits, however, suggests that other roles are likely.Short-term synaptic depression and facilitation at particular synapses are often elicited by different temporal patterns of activity. This differential frequency dependence can, therefore, contribute to translating different temporal patterns of activity into differing amplitudes of postsynaptic responses, i.e., temporal fil...

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Responses of electrosensory neurons in the torus semicircularis of Eigenmannia to complex beat stimuli: testing hypotheses of temporal filtering

Cited by 8 publications

References 32 publications

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Frequency-Dependent PSP Depression Contributes to Low-Pass Temporal Filtering inEigenmannia

Short-Term Synaptic Plasticity Contributes to the Temporal Filtering of Electrosensory Information

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