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

Abstract

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.

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

“…Indeed, recent studies have shown that the statistics of movement envelopes will change as a function of the animal's environment (Huang et al . 2019). Specifically, these are determined from the relative movement between two or more conspecifics; the animal's level of activity will strongly determine how steeply spectral power decays with increasing temporal frequency (i.e.…”

Neural Synchrony Gives Rise to Amplitude- and Duration-Invariant Encoding Consistent With Perception of Natural Communication Stimuli

“…This is particularly important as previous studies have shown that a strong factor contributing to PCell heterogeneities is the amount of descending input (i.e., feedback) that is received from higher brain centers. The effect of such feedback has been mostly studied at the single neuron level (Bastian, 1986;Chacron et al, 2005b;Marsat and Maler, 2012;Huang et al, 2018Huang et al, , 2019Metzen et al, 2018) and further studies are needed to understand whether and, if so, how such feedback can facilitate detection of EA synchrony by ELL PCells.…”

Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons

“…Glutamate (1 mM; Sigma-Aldrich) and serotonin (1 mM; Sigma-Aldrich) were dissolved in saline (111 mM NaCl, 2 mM KCl, 2 mM CaCl 2 , 1 mM MgSO 4 , 1 mM NaHCO 3 and 0.5 mM NaH 2 PO 4 ; Sigma-Aldrich) for application. Drug application electrodes were made using either two-barrel (for electrophysiology) or single-barrel (for behavior) glass micropipettes as described previously (Huang et al, 2018 , 2019 ; Marquez and Chacron, 2018 , 2020b ; Metzen et al, 2018 ). For single neuron recordings, two-barrel pipettes were used for independent application of serotonin or glutamate in the vicinity of the neuron being recorded.…”

“…Specifically, when two fish are located close to one another (i.e., <1 m apart), interference between their EODs gives rise to sinusoidal amplitude modulation (AM) whose frequency is given by the difference between the EOD frequencies. Changes in the relative orientation and distance between both animals give rise to changes in the amplitude (i.e., the envelope) of the sinusoidal amplitude modulation (Yu et al, 2012 ; Fotowat et al, 2013 ; Metzen and Chacron, 2014 ; Huang et al, 2019 ). As such, the frequency components of the envelope are directly associated with the statistics of the relative movement between fish.…”