scholarly journals Nonlinear Information Processing in a Model Sensory System

2006 ◽  
Vol 95 (5) ◽  
pp. 2933-2946 ◽  
Author(s):  
Maurice J. Chacron
Keyword(s):  
Pyramidal Cell ◽  
Sensory System ◽  
Sensory Information ◽  
Pyramidal Cells ◽  
Spike Trains ◽  
Weakly Electric Fish ◽  
Synaptic Noise ◽  
Optimal Linear ◽  
Pharmacological Blockade ◽  
Weakly Electric

Understanding the mechanisms by which sensory neurons encode and decode information remains an important goal in neuroscience. We quantified the performance of optimal linear and nonlinear encoding models in a well-characterized sensory system: the electric sense of weakly electric fish. We show that linear encoding models generally perform better under spatially localized stimulation than under spatially diffuse stimulation. Through pharmacological blockade of feedback input and spatial saturation of the receptive field center, we show that there is significantly less synaptic noise under spatially diffuse stimuli as compared with spatially localized stimuli. Modeling results suggest that pyramidal cells nonlinearly encode sensory information through shunting in their dendrites and clarify the influence of synaptic noise on the performance of linear encoding models. Finally, we used information theory to quantify the performance of linear decoders. While the optimal linear decoder for spatially localized stimuli could capture 60% of the information in pyramidal cell spike trains, the optimal linear decoder for spatially diffuse stimuli could only capture 40% of the information. These results show that nonlinear decoders are necessary to fully access information in pyramidal cell spike trains, and we discuss potential mechanisms by which higher-order neurons could decode this information.

scholarly journals Persistent Na+ Current Modifies Burst Discharge By Regulating Conditional Backpropagation of Dendritic Spikes

2003 ◽  
Vol 89 (1) ◽  
pp. 324-337 ◽  
Author(s):  
Brent Doiron ◽  
Liza Noonan ◽  
Neal Lemon ◽  
Ray W. Turner
Keyword(s):  
Sodium Current ◽  
Pyramidal Cells ◽  
Weakly Electric Fish ◽  
Burst Frequency ◽  
Burst Discharge ◽  
Dendritic Spikes ◽  
Dendritic Spike ◽  
Time Required ◽  
Weakly Electric ◽  
Spike Bursts

The estimation and detection of stimuli by sensory neurons is affected by factors that govern a transition from tonic to burst mode and the frequency chracteristics of burst output. Pyramidal cells in the electrosensory lobe of weakly electric fish generate spike bursts for the purpose of stimulus detection. Spike bursts are generated during repetitive discharge when a frequency-dependent broadening of dendritic spikes increases current flow from dendrite to soma to potentiate a somatic depolarizing afterpotential (DAP). The DAP eventually triggers a somatic spike doublet with an interspike interval that falls inside the dendritic refractory period, blocking spike backpropagiation and the DAP. Repetition of this process gives rise to a rhythmic dendritic spike failure, termed conditional backpropagation, that converts cell output from tonic to burst discharge. Through in vitrorecordings and compartmental modeling we show that burst frequency is regulated by the rate of DAP potentiation during a burst, which determines the time required to discharge the spike doublet that blocks backpropagation. DAP potentiation is maginfied through a postitve feedback process when an increase in dendritic spike duration activates persistent sodium current ( I NaP). I NaP further promotes a slow depolarization that induces a shift from tonic to burst discharge over time. The results are consistent with a dynamical systems analysis that shows that the threshold separating tonic and burst discharge can be represented as a saddle-node bifurcation. The interaction between dendritic K+ current and I NaP provides a physiological explanation for a variable time scale of bursting dynamics characteristic of such a bifurcation.

Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe

1999 ◽  
Vol 202 (10) ◽  
pp. 1255-1265 ◽  
Author(s):  
R.W. Turner ◽  
L. Maler
Keyword(s):  
Feature Extraction ◽  
Lateral Line ◽  
Pyramidal Cell ◽  
Frequency Tuning ◽  
Pyramidal Cells ◽  
Weakly Electric Fish ◽  
Burst Discharge ◽  
Sensory Maps

Oscillatory and burst discharge is recognized as a key element of signal processing from the level of receptor to cortical output cells in most sensory systems. The relevance of this activity for electrosensory processing has become increasingly apparent for cells in the electrosensory lateral line lobe (ELL) of gymnotiform weakly electric fish. Burst discharge by ELL pyramidal cells can be recorded in vivo and has been directly associated with feature extraction of electrosensory input. In vivo recordings have also shown that pyramidal cells are differentially tuned to the frequency of amplitude modulations across three ELL topographic maps of electroreceptor distribution. Pyramidal cell recordings in vitro reveal two forms of oscillatory discharge with properties consistent with pyramidal cell frequency tuning in vivo. One is a slow oscillation of spike discharge arising from local circuit interactions that exhibits marked changes in several properties across the sensory maps. The second is a fast, intrinsic form of burst discharge that incorporates a newly recognized interaction between somatic and dendritic membranes. These findings suggest that a differential regulation of oscillatory discharge properties across sensory maps may underlie frequency tuning in the ELL and influence feature extraction in vivo.

scholarly journals Balanced ionotropic receptor dynamics support signal estimation via voltage-dependent membrane noise

2016 ◽  
Vol 115 (1) ◽  
pp. 530-545 ◽  
Author(s):  
Curtis M. Marcoux ◽  
Stephen E. Clarke ◽  
William H. Nesse ◽  
Andre Longtin ◽  
Leonard Maler
Keyword(s):  
Pyramidal Cell ◽  
Pyramidal Neurons ◽  
Dynamic Balance ◽  
Significant Proportion ◽  
Low Frequency ◽  
Pyramidal Cells ◽  
Weakly Electric Fish ◽  
Ionotropic Receptor ◽  
Membrane Noise ◽  
Voltage Dependent

Encoding behaviorally relevant stimuli in a noisy background is critical for animals to survive in their natural environment. We identify core biophysical and synaptic mechanisms that permit the encoding of low-frequency signals in pyramidal neurons of the weakly electric fish Apteronotus leptorhynchus, an animal that can accurately encode even miniscule amplitude modulations of its self-generated electric field. We demonstrate that slow NMDA receptor (NMDA-R)-mediated excitatory postsynaptic potentials (EPSPs) are able to summate over many interspike intervals (ISIs) of the primary electrosensory afferents (EAs), effectively eliminating the baseline EA ISI correlations from the pyramidal cell input. Together with a dynamic balance of NMDA-R and GABA-A-R currents, this permits stimulus-evoked changes in EA spiking to be transmitted efficiently to target electrosensory lobe (ELL) pyramidal cells, for encoding low-frequency signals. Interestingly, AMPA-R activity is depressed and appears to play a negligible role in the generation of action potentials. Instead, we hypothesize that cell-intrinsic voltage-dependent membrane noise supports the encoding of perithreshold sensory input; this noise drives a significant proportion of pyramidal cell spikes. Together, these mechanisms may be sufficient for the ELL to encode signals near the threshold of behavioral detection.

Oscillatory and burst discharge across electrosensory topographic maps

1996 ◽  
Vol 76 (4) ◽  
pp. 2364-2382 ◽  
Author(s):  
R. W. Turner ◽  
J. R. Plant ◽  
L. Maler
Keyword(s):  
Electric Fields ◽  
Pyramidal Cell ◽  
Unit Activity ◽  
Pyramidal Cells ◽  
Average Frequency ◽  
Afferent Input ◽  
Weakly Electric Fish ◽  
Burst Discharge

1. Three parallel maps of the distribution of tuberous electroreceptor inputs are found in the medullary electrosensory lateral line lobe (ELL) of weakly electric fish. Pyramidal cells in each map are known to respond differentially to the frequency of amplitude modulations (AMs) of external electric fields in vivo. We used an in vitro ELL slice preparation of Apteronotus leptorhynchus to compare the characteristics of spontaneously active single units across the three tuberous maps. It was our objective to determine whether spontaneous bursting activity of pyramidal cells in each map correlates with the known AM frequency selectivities of pyramidal cells in vivo. 2. Single-unit discharges were recorded from the pyramidal cell layer of the centromedial segment (CMS), centrolateral segment (CLS), and lateral segment (LS) of the ELL. Stochastic analysis of interspike intervals (ISIs) was used to identify bursting and nonbursting unit activity, and to separately analyze intra- and interburst ISIs. Four ISI patterns were identified as 1) bursting, 2) regular spiking, 3) irregular spiking, and 4) highly irregular spiking. This work focuses primarily on the characteristics of bursting units across the ELL segments. 3. Spontaneous bursting discharge was identified in all three maps (68 of 97 units), with several characteristics changing in a gradual manner across the maps. The coefficient of variation (CV) of ISIs and intraburst ISIs decreased significantly from the CMS to the LS, whereas the CV of burst periods increased significantly from the CMS to the LS. Autocorrelations and power spectral density analysis identified units discharging in an oscillatory manner with the following ratio: CMS, 75%; CLS, 4%; LS, 8%. 4. The mean period of spike bursts decreased significantly across the segments (CMS, 2.7 s; CLS, 1.2 s; LS, 1.1 s) primarily because of a shortening of mean burst duration (CMS, 1.0 s; CLS, 0.1 s; LS, 0.05 s). The average number of spikes per burst decreased significantly across the maps (CMS, 61; CLS, 8; LS, 8), whereas the average frequency of spikes per burst increased (CMS, 90 Hz; CLS, 130 Hz; LS, 178 Hz), mainly through an increase in the maximal frequencies attained by units within each map. 5. Bursts in the CMS were unstructured in that the intraburst ISIs were serially independent, whereas for many units in the CLS and especially the LS there were serial dependencies of successive spikes, with alternating short and long ISIs during the burst. 6. These data reveal that the characteristics of bursting unit activity differ between the CMS, CLS, and LS maps in vitro, implying a modulation of the factors underlying burst discharge across multiple sensory maps. Because the pattern of change in burst activity between these maps parallels that of pyramidal cell AM frequency selectivity in vivo, oscillatory and burst discharge may represent the cellular mechanism used to tune these cells to specific frequencies of afferent input during electrolocation and electrocommunication.

Interval Coding. I. Burst Interspike Intervals as Indicators of Stimulus Intensity

2007 ◽  
Vol 97 (4) ◽  
pp. 2731-2743 ◽  
Author(s):  
Anne-Marie M. Oswald ◽  
Brent Doiron ◽  
Leonard Maler
Keyword(s):  
Stimulus Intensity ◽  
Information Transfer ◽  
Pyramidal Cells ◽  
Sensory Stimulation ◽  
Weakly Electric Fish ◽  
Interspike Intervals ◽  
Direct Stimulation ◽  
Distinct Features ◽  
Weakly Electric

Short interspike intervals such as those that occur during burst firing are hypothesized to be distinct features of the neural code. Although a number of correlations between the occurrence of burst events and aspects of the stimulus have been identified, the relationship between burst characteristics and information transfer is uncertain. Pyramidal cells in the electrosensory lobe of the weakly electric fish, Apteronotus leptorhynchus, respond to dynamic broadband electrosensory stimuli with bursts and isolated spikes. In the present study, we mimic synaptic input during sensory stimulation by direct stimulation of electrosensory pyramidal cells with broadband current in vitro. The pyramidal cells respond to this stimulus with burst interspike intervals (ISIs) that are reliably and precisely correlated with the intensity of stimulus upstrokes. We found burst ISIs must differ by a minimum of 2 ms to discriminate, with low error, differences in stimulus intensity. Based on these results, we define and quantify a candidate interval code for the processing of sensory input. Finally, we demonstrate that interval coding is restricted to short ISIs such as those generated in burst events and that the proposed interval code is distinct from rate and timing codes.

Communication with self, friends and foes in active-sensing animals

2021 ◽  
Vol 224 (22) ◽  
Author(s):  
Te K. Jones ◽  
Kathryne M. Allen ◽  
Cynthia F. Moss
Keyword(s):  
Electric Fish ◽  
Prey Capture ◽  
Sensory Information ◽  
Weakly Electric Fish ◽  
Active Sensing ◽  
Sensing Systems ◽  
Risk Of Predation ◽  
Evolutionary Success ◽  
Specialized Form ◽  
Weakly Electric

ABSTRACT Animals that rely on electrolocation and echolocation for navigation and prey detection benefit from sensory systems that can operate in the dark, allowing them to exploit sensory niches with few competitors. Active sensing has been characterized as a highly specialized form of communication, whereby an echolocating or electrolocating animal serves as both the sender and receiver of sensory information. This characterization inspires a framework to explore the functions of sensory channels that communicate information with the self and with others. Overlapping communication functions create challenges for signal privacy and fidelity by leaving active-sensing animals vulnerable to eavesdropping, jamming and masking. Here, we present an overview of active-sensing systems used by weakly electric fish, bats and odontocetes, and consider their susceptibility to heterospecific and conspecific jamming signals and eavesdropping. Susceptibility to interference from signals produced by both conspecifics and prey animals reduces the fidelity of electrolocation and echolocation for prey capture and foraging. Likewise, active-sensing signals may be eavesdropped, increasing the risk of alerting prey to the threat of predation or the risk of predation to the sender, or drawing competition to productive foraging sites. The evolutionary success of electrolocating and echolocating animals suggests that they effectively counter the costs of active sensing through rich and diverse adaptive behaviors that allow them to mitigate the effects of competition for signal space and the exploitation of their signals.

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