scholarly journals Descending pathways mediate adaptive optimized coding of natural stimuli in weakly electric fish

2019 ◽  
Vol 5 (10) ◽  
pp. eaax2211 ◽  
Author(s):  
Chengjie G. Huang ◽  
Michael G. Metzen ◽  
Maurice J. Chacron
Keyword(s):  
Environmental Changes ◽  
Behavioral Responses ◽  
Sensory Systems ◽  
Weakly Electric Fish ◽  
Descending Pathways ◽  
Natural Stimuli ◽  
Central Neurons ◽  
Power Spectral ◽  
Underlying Mechanisms ◽  
Weakly Electric

Biological systems must be flexible to environmental changes to survive. This is exemplified by the fact that sensory systems continuously adapt to changes in the environment to optimize coding and behavioral responses. However, the nature of the underlying mechanisms remains poorly understood in general. Here, we investigated the mechanisms mediating adaptive optimized coding of naturalistic stimuli with varying statistics depending on the animal’s velocity during movement. We found that central neurons adapted their responses to stimuli with different power spectral densities such as to optimally encode them, thereby ensuring that behavioral responses are, in turn, better matched to the new stimulus statistics. Sensory adaptation further required descending inputs from the forebrain as well as the raphe nuclei. Our findings thus reveal a previously unknown functional role for descending pathways in mediating adaptive optimized coding of natural stimuli that is likely generally applicable across sensory systems and species.

scholarly journals Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish

2011 ◽  
Vol 106 (6) ◽  
pp. 3102-3118 ◽  
Author(s):  
Katrin Vonderschen ◽  
Maurice J. Chacron
Keyword(s):  
Sparse Coding ◽  
Electric Fish ◽  
Neural Representation ◽  
Weakly Electric Fish ◽  
Torus Semicircularis ◽  
Dense Coding ◽  
Natural Stimuli ◽  
Central Neurons ◽  
Weakly Electric ◽  
Peripheral Sensory

While peripheral sensory neurons respond to natural stimuli with a broad range of spatiotemporal frequencies, central neurons instead respond sparsely to specific features in general. The nonlinear transformations leading to this emergent selectivity are not well understood. Here we characterized how the neural representation of stimuli changes across successive brain areas, using the electrosensory system of weakly electric fish as a model system. We found that midbrain torus semicircularis (TS) neurons were on average more selective in their responses than hindbrain electrosensory lateral line lobe (ELL) neurons. Further analysis revealed two categories of TS neurons: dense coding TS neurons that were ELL-like and sparse coding TS neurons that displayed selective responses. These neurons in general responded to preferred stimuli with few spikes and were mostly silent for other stimuli. We further investigated whether information about stimulus attributes was contained in the activities of ELL and TS neurons. To do so, we used a spike train metric to quantify how well stimuli could be discriminated based on spiking responses. We found that sparse coding TS neurons performed poorly even when their activities were combined compared with ELL and dense coding TS neurons. In contrast, combining the activities of as few as 12 dense coding TS neurons could lead to optimal discrimination. On the other hand, sparse coding TS neurons were better detectors of whether their preferred stimulus occurred compared with either dense coding TS or ELL neurons. Our results therefore suggest that the TS implements parallel detection and estimation of sensory input.

scholarly journals Population Coding by Electrosensory Neurons

2008 ◽  
Vol 99 (4) ◽  
pp. 1825-1835 ◽  
Author(s):  
Maurice J. Chacron ◽  
Joseph Bastian
Keyword(s):  
Time Window ◽  
Population Coding ◽  
Weakly Electric Fish ◽  
Critical Feature ◽  
Sensory Stimuli ◽  
Biologically Relevant ◽  
Central Neurons ◽  
Correlated Activity ◽  
The Individual ◽  
Weakly Electric

Sensory stimuli typically activate many receptors at once and therefore should lead to increases in correlated activity among central neurons. Such correlated activity could be a critical feature in the encoding and decoding of information in central circuits. Here we characterize correlated activity in response to two biologically relevant classes of sensory stimuli in the primary electrosensory nuclei, the electrosensory lateral line lobe, of the weakly electric fish Apteronotus leptorhynchus. Our results show that these neurons can display significant correlations in their baseline activities that depend on the amount of receptive field overlap. A detailed analysis of spike trains revealed that correlated activity resulted predominantly from a tendency to fire synchronous or anti-synchronous bursts of spikes. We also explored how different stimulation protocols affected correlated activity: while prey-like stimuli increased correlated activity, conspecific-like stimuli decreased correlated activity. We also computed the correlations between the variabilities of each neuron to repeated presentations of the same stimulus (noise correlations) and found lower amounts of noise correlation for communication stimuli. Therefore the decrease in correlated activity seen with communication stimuli is caused at least in part by reduced noise correlations. This differential modulation in correlated activity occurred because of changes in burst firing at the individual neuron level. Our results show that different categories of behaviorally relevant input will differentially affect correlated activity. In particular, we show that the number of correlated bursts within a given time window could be used by postsynaptic neurons to distinguish between both stimulus categories.

scholarly journals Neural correlations enable invariant coding and perception of natural stimuli in weakly electric fish

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Michael G Metzen ◽  
Volker Hofmann ◽  
Maurice J Chacron
Keyword(s):  
Electric Fish ◽  
Neural Circuit ◽  
Neural Representation ◽  
Weakly Electric Fish ◽  
Relevant Stimulus ◽  
Invariant Representation ◽  
Natural Stimuli ◽  
Neural Representations ◽  
Stimulus Features ◽  
Weakly Electric

Neural representations of behaviorally relevant stimulus features displaying invariance with respect to different contexts are essential for perception. However, the mechanisms mediating their emergence and subsequent refinement remain poorly understood in general. Here, we demonstrate that correlated neural activity allows for the emergence of an invariant representation of natural communication stimuli that is further refined across successive stages of processing in the weakly electric fish Apteronotus leptorhynchus. Importantly, different patterns of input resulting from the same natural communication stimulus occurring in different contexts all gave rise to similar behavioral responses. Our results thus reveal how a generic neural circuit performs an elegant computation that mediates the emergence and refinement of an invariant neural representation of natural stimuli that most likely constitutes a neural correlate of perception.

scholarly journals Feedback optimizes neural coding and perception of natural stimuli

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Chengjie G Huang ◽  
Michael G Metzen ◽  
Maurice J Chacron
Keyword(s):  
Neural Coding ◽  
Spectral Power ◽  
Tuning Curve ◽  
Weakly Electric Fish ◽  
Neural Responses ◽  
Low Frequencies ◽  
Natural Stimuli ◽  
Descending Input ◽  
Underlying Mechanisms ◽  
High Pass

Growing evidence suggests that sensory neurons achieve optimal encoding by matching their tuning properties to the natural stimulus statistics. However, the underlying mechanisms remain unclear. Here we demonstrate that feedback pathways from higher brain areas mediate optimized encoding of naturalistic stimuli via temporal whitening in the weakly electric fish Apteronotus leptorhynchus. While one source of direct feedback uniformly enhances neural responses, a separate source of indirect feedback selectively attenuates responses to low frequencies, thus creating a high-pass neural tuning curve that opposes the decaying spectral power of natural stimuli. Additionally, we recorded from two populations of higher brain neurons responsible for the direct and indirect descending inputs. While one population displayed broadband tuning, the other displayed high-pass tuning and thus performed temporal whitening. Hence, our results demonstrate a novel function for descending input in optimizing neural responses to sensory input through temporal whitening that is likely to be conserved across systems and species.

Dendritic Na+ Current Inactivation Can Increase Cell Excitability By Delaying a Somatic Depolarizing Afterpotential

2005 ◽  
Vol 94 (6) ◽  
pp. 3836-3848 ◽  
Author(s):  
Fernando R. Fernandez ◽  
W. Hamish Mehaffey ◽  
Ray W. Turner
Keyword(s):  
Pyramidal Cells ◽  
Firing Frequency ◽  
Weakly Electric Fish ◽  
Dynamical Analysis ◽  
Central Neurons ◽  
Electrophysiological Recordings ◽  
A Cell ◽  
Dendritic Spike ◽  
Weakly Electric ◽  
The Relationship

Many central neurons support active dendritic spike backpropagation mediated by voltage-gated currents. Active spikes in dendrites have been shown capable of providing feedback to the soma to influence somatic excitability and firing dynamics through a depolarizing afterpotential (DAP). In pyramidal cells of the electrosensory lobe of weakly electric fish, Na+ spikes in dendrites undergo a frequency-dependent broadening that enhances the DAP to increase somatic firing frequency. We use a combination of dynamical analysis and electrophysiological recordings to demonstrate that spike broadening in dendrites is primarily caused by a cumulative inactivation of dendritic Na+ current. We further show that a reduction in dendritic Na+ current increases excitability by decreasing the interspike interval and promoting burst firing. This process arises when inactivation of dendritic Na+ current shifts the latency of the dendritic spike to delay the arrival of the DAP sufficiently to increase its impact on somatic membrane potential despite a reduction in dendritic excitability. Furthermore, the relationship between dendritic Na+ current density and somatic excitability is nonmonotonic, as intermediate levels of dendritic Na+ current exert the greatest excitatory influence. These results reveal that temporal shifts in dendritic spike firing provide a novel means for backpropagating spikes to influence the final output of a cell.

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