Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish

2017

PLoS ONE

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Neural heterogeneities are seen ubiquitously within the brain and greatly complicate classification efforts. Here we tested whether the responses of an anatomically well-characterized sensory neuron population to natural stimuli could be used for functional classification. To do so, we recorded from pyramidal cells within the electrosensory lateral line lobe (ELL) of the weakly electric fish Apteronotus leptorhynchus in response to natural electro-communication stimuli as these cells can be anatomically classified into six different types. We then used two independent methodologies to functionally classify responses: one relies of reducing the dimensionality of a feature space while the other directly compares the responses themselves. Both methodologies gave rise to qualitatively similar results: while ON and OFF-type cells could easily be distinguished from one another, ELL pyramidal neuron responses are actually distributed along a continuum rather than forming distinct clusters due to heterogeneities. We discuss the implications of our results for neural coding and highlight some potential advantages.

Section: Discussionmentioning

confidence: 99%

Electrosensory neural responses to natural electro-communication stimuli are distributed along a continuum

Sproule

2017

PLoS ONE

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“…ELL pyramidal cells also receive large amounts of neuromodulatory input (Marquez et al . 2013) including serotonergic fibres from the raphe nuclei (Johnston et al . 1990; Deemyad et al .…”

Section: Introductionmentioning

confidence: 99%

Serotonin modulates optimized coding of natural stimuli through increased neural and behavioural responses via enhanced burst firing

Marquez

The Journal of Physiology

2020

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Key pointsr The function of serotonergic fibres onto sensory areas remains poorly understood r We show that serotonin application enhances sensory neural and behavioural responses to second order stimuli r Enhanced neural responses most likely occurred because of increased burst firing r Changes in neural sensitivity due to burst firing were the best predictor of changes in behavioural sensitivity r Our results suggest that serotonin optimizes coding of stimuli encountered during aggression.Abstract Understanding how the processing of sensory information leads to behavioural responses remains a central problem in systems neuroscience. Here, we investigated how the neuromodulator serotonin affects neural and behavioural responses to second-order envelope stimuli within the electrosensory system of the weakly electric fish Apteronotus leptorhynchus. We found that serotonin application increased neuronal excitability through greater tendency for burst firing. We found that increased excitability led to overall higher neural sensitivities to higher envelope frequencies. Separating the spike train into bursts and isolated spike train components revealed that this was due to significant increases in neural sensitivity for the former but not the latter. We next investigated the consequences of such changes in sensitivity towards optimized coding of stimuli with specific statistics. Our results show that serotonin application compromised optimal coding of stimuli with statistics seen under naturalistic conditions due to changes in burst, but not isolated spike firing. Finally, we found that serotonin application increased behavioural sensitivity to envelope stimuli. Interestingly, changes in neural sensitivity due to bursts were a far better predictor of changes in behavioural sensitivity, suggesting that burst firing is decoded by downstream brain areas. Overall, our results suggest that serotonin modulates neural responses to optimize coding and perception of stimuli during behavioural contexts associated with encountering dominant conspecifics. Mariana Marquez is a PhD student in the Physiology department at McGill University. She holds a BS in Physics from the National Autonomous University of Mexico (UNAM) in Mexico City, Mexico. During her undergraduate studies she investigated changes in the neural oscillatory patterns due to homeostatic stress. She currently works on understanding how serotonin modulates neural responses to stimuli in nature.

“…Gymnotiform weakly electric fish generate a quasi-sinusoidal electric field through an electric organ discharge (EOD) and constitute an attractive model system for studying how the brain processes second-order stimulus attributes because of wellcharacterized anatomy and behavior (Chacron et al, 2003;Chacron et al, 2011;Krahe and Maler, 2014;Márquez et al, 2013;Marsat et al, 2012;Stamper et al, 2013). Specific electroreceptors scattered on the skin surface monitor changes in the amplitude of the field (i.e.…”

Section: Introductionmentioning

confidence: 99%

Weakly electric fish give behavioral responses to envelopes naturally occurring during movement: implications for neural processing

Metzen

Journal of Experimental Biology

2013

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102

How the brain processes natural sensory input remains an important and poorly understood problem in neuroscience. The efficient coding hypothesis asserts that the brain's coding strategies are adapted to the statistics of natural stimuli in order to efficiently process them, thereby optimizing their perception by the organism. Here we examined whether gymnotiform weakly electric fish displayed behavioral responses that are adapted to the statistics of the natural electrosensory envelopes. Previous studies have shown that the envelopes resulting from movement tend to consist of low (<1 Hz) temporal frequencies and are behaviorally relevant whereas those resulting from social interactions consist of higher (>1 Hz) temporal frequencies that can thus mask more behaviorally relevant signals. We found that the self-generated electric organ discharge frequency follows the detailed time course of the envelope around a mean value that is positively offset with respect to its baseline value for temporal frequencies between 0.001 Hz and 1 Hz. The frequency-following component of this behavioral response decreased in magnitude as a power law as a function of the envelope frequency and was negligible for envelope frequencies above 1 Hz. In contrast, the offset component was relatively constant and somewhat increased for envelope frequencies above 1 Hz. Thus, our results show that weakly electric fish display behavioral responses that track the detailed time course of low but not high frequency envelope stimuli. Furthermore, we found that the magnitude of the frequency-following behavioral response matches, in a one-to-one fashion, the spectral power of natural second-order stimulus attributes observed during movement. Indeed, both decayed as a power law with the same exponent for temporal frequencies spanning three orders of magnitude. Thus, our findings suggest that the neural coding strategies used by weakly electric fish perceive the detailed time course of movement envelopes and are adapted to their statistics as found in the natural environment. They also suggest that weakly electric fish might take advantage of the differential frequency content of movement and social envelopes in order to give appropriate behavioral responses during encounters between two or more conspecifics.