scholarly journals Inhibition of SK and M channel-mediated currents by 5-HT enables parallel processing by bursts and isolated spikes

2011 ◽  
Vol 105 (3) ◽  
pp. 1276-1294 ◽  
Author(s):  
Tara Deemyad ◽  
Leonard Maler ◽  
Maurice J. Chacron
Keyword(s):  
Pyramidal Neurons ◽  
Sensory Information ◽  
Burst Firing ◽  
Weakly Electric Fish ◽  
Specific Stimulus ◽  
Communication Signals ◽  
Electrophysiological Recordings ◽  
Firing Mode ◽  
Stimulus Features ◽  
Weakly Electric

Although serotonergic innervation of sensory brain areas is ubiquitous, its effects on sensory information processing remain poorly understood. We investigated these effects in pyramidal neurons within the electrosensory lateral line lobe (ELL) of weakly electric fish. Surprisingly, we found that 5-HT is present at different levels across the different ELL maps; the presence of 5-HT fibers was highest in the map that processes intraspecies communication signals. Electrophysiological recordings revealed that 5-HT increased excitability and burst firing through a decreased medium afterhyperpolarization resulting from reduced small-conductance calcium-activated (SK) currents as well as currents mediated by an M-type potassium channel. We next investigated how 5-HT alters responses to sensory input. 5-HT application decreased the rheobase current, increased the gain, and decreased first spike latency. Moreover, it reduced discriminability between different stimuli, as quantified by the mutual information rate. We hypothesized that 5-HT shifts pyramidal neurons into a burst-firing mode where bursts, when considered as events, can detect the presence of particular stimulus features. We verified this hypothesis using signal detection theory. Our results indeed show that serotonin-induced bursts of action potentials, when considered as events, could detect specific stimulus features that were distinct from those detected by isolated spikes. Moreover, we show the novel result that isolated spikes transmit more information after 5-HT application. Our results suggest a novel function for 5-HT in that it enables differential processing by action potential patterns in response to current injection.

scholarly journals Serotonergic modulation across sensory modalities

2020 ◽  
Vol 123 (6) ◽  
pp. 2406-2425
Author(s):  
Tyler R. Sizemore ◽  
Laura M. Hurley ◽  
Andrew M. Dacks
Keyword(s):  
Serotonin Receptor ◽  
Physiological State ◽  
Sensory Information ◽  
Specific Stimulus ◽  
Sensory Organization ◽  
Sensory Modalities ◽  
Multiple Levels ◽  
Stimulus Features ◽  
Ubiquitous Presence ◽  
Serotonergic Modulation

The serotonergic system has been widely studied across animal taxa and different functional networks. This modulatory system is therefore well positioned to compare the consequences of neuromodulation for sensory processing across species and modalities at multiple levels of sensory organization. Serotonergic neurons that innervate sensory networks often bidirectionally exchange information with these networks but also receive input representative of motor events or motivational state. This convergence of information supports serotonin’s capacity for contextualizing sensory information according to the animal’s physiological state and external events. At the level of sensory circuitry, serotonin can have variable effects due to differential projections across specific sensory subregions, as well as differential serotonin receptor type expression within those subregions. Functionally, this infrastructure may gate or filter sensory inputs to emphasize specific stimulus features or select among different streams of information. The near-ubiquitous presence of serotonin and other neuromodulators within sensory regions, coupled with their strong effects on stimulus representation, suggests that these signaling pathways should be considered integral components of sensory systems.

Spike-Timing Precision Underlies the Coding Efficiency of Auditory Receptor Neurons

2006 ◽  
Vol 95 (4) ◽  
pp. 2541-2552 ◽  
Author(s):  
Ariel Rokem ◽  
Sebastian Watzl ◽  
Tim Gollisch ◽  
Martin Stemmler ◽  
Andreas V. M. Herz ◽  
...  
Keyword(s):  
Spike Train ◽  
Spike Trains ◽  
Neural Representation ◽  
Neural Firing ◽  
Specific Stimulus ◽  
Time Jitter ◽  
Information Rates ◽  
Communication Signals ◽  
Receptor Neurons ◽  
Stimulus Features

Sensory systems must translate incoming signals quickly and reliably so that an animal can act successfully in its environment. Even at the level of receptor neurons, however, functional aspects of the sensory encoding process are not yet fully understood. Specifically, this concerns the question how stimulus features and neural response characteristics lead to an efficient transmission of sensory information. To address this issue, we have recorded and analyzed spike trains from grasshopper auditory receptors, while systematically varying the stimulus statistics. The stimulus variations profoundly influenced the efficiency of neural encoding. This influence was largely attributable to the presence of specific stimulus features that triggered remarkably precise spikes whose trial-to-trial timing variability was as low as 0.15 ms—one order of magnitude shorter than typical stimulus time scales. Precise spikes decreased the noise entropy of the spike trains, thereby increasing the rate of information transmission. In contrast, the total spike train entropy, which quantifies the variety of different spike train patterns, hardly changed when stimulus conditions were altered, as long as the neural firing rate remained the same. This finding shows that stimulus distributions that were transmitted with high information rates did not invoke additional response patterns, but instead displayed exceptional temporal precision in their neural representation. The acoustic stimuli that led to the highest information rates and smallest spike-time jitter feature pronounced sound-pressure deflections lasting for 2–3 ms. These upstrokes are reminiscent of salient structures found in natural grasshopper communication signals, suggesting that precise spikes selectively encode particularly important aspects of the natural stimulus environment.

scholarly journals Dendritic Voltage-Gated Ion Channels Regulate the Action Potential Firing Mode of Hippocampal CA1 Pyramidal Neurons

1999 ◽  
Vol 82 (4) ◽  
pp. 1895-1901 ◽  
Author(s):  
Jeffrey C. Magee ◽  
Michael Carruth
Keyword(s):  
Ion Channels ◽  
Action Potential ◽  
Large Amplitude ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Burst Firing ◽  
Voltage Gated ◽  
Ca1 Pyramidal Neurons ◽  
Firing Mode ◽  
Voltage Gated Ion Channels

The role of dendritic voltage-gated ion channels in the generation of action potential bursting was investigated using whole cell patch-clamp recordings from the soma and dendrites of CA1 pyramidal neurons located in hippocampal slices of adult rats. Under control conditions somatic current injections evoked single action potentials that were associated with an afterhyperpolarization (AHP). After localized application of 4-aminopyridine (4-AP) to the distal apical dendritic arborization, the same current injections resulted in the generation of an afterdepolarization (ADP) and multiple action potentials. This burst firing was not observed after localized application of 4-AP to the soma/proximal dendrites. The dendritic 4-AP application allowed large-amplitude Na+-dependent action potentials, which were prolonged in duration, to backpropagate into the distal apical dendrites. No change in action potential backpropagation was seen with proximal 4-AP application. Both the ADP and action potential bursting could be inhibited by the bath application of nonspecific concentrations of divalent Ca2+ channel blockers (NiCl and CdCl). Ca2+ channel blockade also reduced the dendritic action potential duration without significantly affecting spike amplitude. Low concentrations of TTX (10–50 nM) also reduced the ability of the CA1 neurons to fire in the busting mode. This effect was found to be the result of an inhibition of backpropagating dendritic action potentials and could be overcome through the coordinated injection of transient, large-amplitude depolarizing current into the dendrite. Dendritic current injections were able to restore the burst firing mode (represented as a large ADP) even in the presence of high concentrations of TTX (300–500 μM). These data suggest the role of dendritic Na+ channels in bursting is to allow somatic/axonal action potentials to backpropagate into the dendrites where they then activate dendritic Ca2+ channels. Although it appears that most Ca2+ channel subtypes are important in burst generation, blockade of T- and R-type Ca2+ channels by NiCl (75 μM) inhibited action potential bursting to a greater extent than L-channel (10 μM nimodipine) or N-, P/Q-type (1 μM ω-conotoxin MVIIC) Ca2+ channel blockade. This suggest that the Ni-sensitive voltage-gated Ca2+ channels have the most important role in action potential burst generation. In summary, these data suggest that the activation of dendritic voltage-gated Ca2+ channels, by large-amplitude backpropagating spikes, provides a prolonged inward current that is capable of generating an ADP and burst of multiple action potentials in the soma of CA1 pyramidal neurons. Dendritic voltage-gated ion channels profoundly regulate the processing and storage of incoming information in CA1 pyramidal neurons by modulating the action potential firing mode from single spiking to burst firing.

Encoding of social signals in all three electrosensory pathways of Eigenmannia virescens

2014 ◽  
Vol 112 (9) ◽  
pp. 2076-2091 ◽  
Author(s):  
Anna Stöckl ◽  
Fabian Sinz ◽  
Jan Benda ◽  
Jan Grewe
Keyword(s):  
Weakly Electric Fish ◽  
Social Signals ◽  
Active System ◽  
Behavioral Experiments ◽  
Communication Signals ◽  
Parallel Pathways ◽  
Electrophysiological Recordings ◽  
Eigenmannia Virescens ◽  
Neuronal Representation

Extracting complementary features in parallel pathways is a widely used strategy for a robust representation of sensory signals. Weakly electric fish offer the rare opportunity to study complementary encoding of social signals in all of its electrosensory pathways. Electrosensory information is conveyed in three parallel pathways: two receptor types of the tuberous (active) system and one receptor type of the ampullary (passive) system. Modulations of the fish's own electric field are sensed by these receptors and used in navigation, prey detection, and communication. We studied the neuronal representation of electric communication signals (called chirps) in the ampullary and the two tuberous pathways of Eigenmannia virescens. We first characterized different kinds of chirps observed in behavioral experiments. Since Eigenmannia chirps simultaneously drive all three types of receptors, we studied their responses in in vivo electrophysiological recordings. Our results demonstrate that different electroreceptor types encode different aspects of the stimuli and each appears best suited to convey information about a certain chirp type. A decoding analysis of single neurons and small populations shows that this specialization leads to a complementary representation of information in the tuberous and ampullary receptors. This suggests that a potential readout mechanism should combine information provided by the parallel processing streams to improve chirp detectability.

scholarly journals Selective and Context-Dependent Social and Behavioral Effects of Δ9-Tetrahydrocannabinol in Weakly Electric Fish

2018 ◽  
Vol 91 (4) ◽  
pp. 214-227
Author(s):  
Brandon Neeley ◽  
Tyler Overholt ◽  
Emily Artz ◽  
Steven G. Kinsey ◽  
Gary Marsat
Keyword(s):  
Electric Fish ◽  
Behavioral Effects ◽  
Weakly Electric Fish ◽  
Control Fish ◽  
Dependent Manner ◽  
Neural Basis ◽  
Communication Signals ◽  
Neurophysiological Studies ◽  
Context Dependent ◽  
Weakly Electric

Cannabinoid (CB) receptors are widespread in the nervous system and influence a variety of behaviors. Weakly electric fish have been a useful model system in the study of the neural basis of behavior, but we know nothing of the role played by the CB system. Here, we determine the overall behavioral effect of a nonselective CB receptor agonist, namely Δ9-tetrahydrocannabinol (THC), in the weakly electric fish Apte­ronotus leptorhynchus. Using various behavioral paradigms involving social stimuli, we show that THC decreases locomotor behavior, as in many species, and influences communication and social behavior. Across the different experiments, we found that the propensity to emit communication signals (chirps) and seek social interactions was affected in a context-dependent manner. We explicitly tested this hypothesis by comparing the behavioral effects of THC injection in fish placed in a novel versus a familiar social and physical environment. THC-injected fish were less likely to chirp than control fish in familiar situations but not in novel ones. The tendency to be in close proximity to other fish was affected only in novel environments, with control fish clustering more than THC-injected ones. By identifying behaviors affected by CB agonists, our study can guide further comparative and neurophysiological studies of the role of the CB system using a weakly electric fish as a model.

scholarly journals Stimulus background influences phase invariant coding by correlated neural activity

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Michael G Metzen ◽  
Maurice J Chacron
Keyword(s):  
Phase Locking ◽  
Low Frequency ◽  
Weakly Electric Fish ◽  
Neuron Activity ◽  
Invariant Representation ◽  
Communication Signals ◽  
Correlated Activity ◽  
Peripheral Afferents ◽  
And Behavior ◽  
Weakly Electric

Previously we reported that correlations between the activities of peripheral afferents mediate a phase invariant representation of natural communication stimuli that is refined across successive processing stages thereby leading to perception and behavior in the weakly electric fish Apteronotus leptorhynchus (Metzen et al., 2016). Here, we explore how phase invariant coding and perception of natural communication stimuli are affected by changes in the sinusoidal background over which they occur. We found that increasing background frequency led to phase locking, which decreased both detectability and phase invariant coding. Correlated afferent activity was a much better predictor of behavior as assessed from both invariance and detectability than single neuron activity. Thus, our results provide not only further evidence that correlated activity likely determines perception of natural communication signals, but also a novel explanation as to why these preferentially occur on top of low frequency as well as low-intensity sinusoidal backgrounds.

scholarly journals Distinct lateral inhibitory circuits drive parallel processing of sensory information in the mammalian olfactory bulb

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Matthew A Geramita ◽  
Shawn D Burton ◽  
Nathan N Urban
Keyword(s):  
Granule Cells ◽  
Sensory Information ◽  
Cell Types ◽  
Specific Stimulus ◽  
Inhibitory Circuits ◽  
Parallel Pathways ◽  
Common Strategy ◽  
Feature Selectivity ◽  
Tufted Cells ◽  
Stimulus Features

Splitting sensory information into parallel pathways is a common strategy in sensory systems. Yet, how circuits in these parallel pathways are composed to maintain or even enhance the encoding of specific stimulus features is poorly understood. Here, we have investigated the parallel pathways formed by mitral and tufted cells of the olfactory system in mice and characterized the emergence of feature selectivity in these cell types via distinct lateral inhibitory circuits. We find differences in activity-dependent lateral inhibition between mitral and tufted cells that likely reflect newly described differences in the activation of deep and superficial granule cells. Simulations show that these circuit-level differences allow mitral and tufted cells to best discriminate odors in separate concentration ranges, indicating that segregating information about different ranges of stimulus intensity may be an important function of these parallel sensory pathways.

scholarly journals Neural processing of communication signals: The extent of sender-receiver matching varies across species of Apteronotus

2018 ◽  
Author(s):  
K.M. Allen ◽  
G. Marsat
Keyword(s):  
Central Nervous System ◽  
Nervous System ◽  
Related Species ◽  
Electric Fish ◽  
Weakly Electric Fish ◽  
Closely Related Species ◽  
Communication Signals ◽  
Coding Strategies ◽  
The Central Nervous System ◽  
Weakly Electric

ABSTRACTAs communication signal properties change, through genetic drift or selective pressure, the sensory systems that receive these signals must also adapt to maintain sensitivity and adaptability in an array of contexts. Shedding light on this process helps us understand how sensory codes are tailored to specific tasks. In a species of weakly electric fish, Apteronotus albifrons, we examined the unique neurophysiological properties that support the encoding of electrosensory communication signals that the animal encounters in social exchanges. We compare our findings to known coding properties of the closely related species, Apteronotus leptorhynchus, to establish how these animals differ in their ability to encode their distinctive communication signals. While there are many similarities between these two species, we found notable differences leading to relatively poor coding of the details of chirp structure occurring on high-frequency background beats. As a result, small differences in chirp properties are poorly resolved by the nervous system. We performed behavioral tests to relate A. albifrons chirp coding strategies to its use of chirps during social encounters. Our results suggest that A. albifrons do not exchange frequent chirps in non-breeding condition, particularly when the beat frequency is high. These findings parallel the mediocre chirp coding accuracy in that they both point to a reduced reliance on frequent and rich exchange of information through chirps during these social interactions. Therefore, our study suggests that neural coding strategies in the central nervous system vary across species in a way that parallels the behavioral use of the sensory signals.SIGNIFICANCESender-receiver matching is a phenomenon commonly observed in the peripheral nervous system. It enables communication production and reception to evolve together so that conspecifics remain sensitive to important signals. In this manuscript we examine this phenomenon in the central nervous system of the weakly electric fish A. albifrons and compare its processing of communication signals to a closely related species (A. leptorhynchus). Although some differences across the two species can help tailor the system for processing species-specific signals, our data indicate that encoding of communication signals in A. albifrons is not as sensitive as in A. leptorhynchus for certain categories of signals. Our data support the idea that the extent of sender-receiver matching can vary as a function of behavioral needs.

scholarly journals Selective and context-dependent social and behavioral effects of Δ9-tetrahydrocannabinol in weakly electric fish

2018 ◽  
Author(s):  
Brandon Neeley ◽  
Tyler Overholt ◽  
Emily Artz ◽  
Steven G Kinsey ◽  
Gary Marsat
Keyword(s):  
Electric Fish ◽  
Behavioral Effects ◽  
Weakly Electric Fish ◽  
Control Fish ◽  
Dependent Manner ◽  
Neural Basis ◽  
Communication Signals ◽  
Neurophysiological Studies ◽  
Context Dependent ◽  
Weakly Electric

AbstractCannabinoid (CB) receptors are widespread in the nervous system and influence a variety of behaviors. Weakly electric fish has been a useful model system in the study of the neural basis of behavior but we know nothing of the role played by the CB system. Here, we determine the overall behavioral effect of a CB receptor agonist (i.e., Δ9-tetrahydrocannabinol, THC) in the weakly electric fish A. leptorhynchus. Using various behavioral paradigms involving social stimuli, we show that THC decreases locomotor behavior as in many species and influences the communication and social behavior. Across the different experiments we found that the propensity to emit communication signals (chirps) and to seek social interactions was affected in a context-dependent manner. We explicitly tested this hypothesis by comparing the behavioral effects of THC injection in fish placed in a novel versus familiar social and physical environments. THC-injected fish were less likely to chirp than control in familiar situation but not in novel ones. The tendency to be in close proximity was affected only in novel environments whith control fish clustering more than THC-injected ones. By identifying behaviors affected by CB agonists, our study can guide further comparative and neurophysiological studies of the role of the CB system using weakly electric fish as a model.

Sign in / Sign up

Export Citation Format

Share Document