Descending pathways generate perception of and neural responses to weak sensory input

Abstract

Natural sensory stimuli frequently consist of a fast time-varying waveform whose amplitude or contrast varies more slowly. While changes in contrast carry behaviorally relevant information necessary for sensory perception, their processing by the brain remains poorly understood to this day. Here, we investigated the mechanisms that enable neural responses to and perception of low-contrast stimuli in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus. We found that fish reliably detected such stimuli via robust behavioral responses. Recordings from peripheral electrosensory neurons revealed stimulus-induced changes in firing activity (i.e., phase locking) but not in their overall firing rate. However, central electrosensory neurons receiving input from the periphery responded robustly via both phase locking and increases in firing rate. Pharmacological inactivation of feedback input onto central electrosensory neurons eliminated increases in firing rate but did not affect phase locking for central electrosensory neurons in response to low-contrast stimuli. As feedback inactivation eliminated behavioral responses to these stimuli as well, our results show that it is changes in central electrosensory neuron firing rate that are relevant for behavior, rather than phase locking. Finally, recordings from neurons projecting directly via feedback to central electrosensory neurons revealed that they provide the necessary input to cause increases in firing rate. Our results thus provide the first experimental evidence that feedback generates both neural and behavioral responses to low-contrast stimuli that are commonly found in the natural environment.

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

“…2018; Metzen et al . 2018), terminate on their apical dendrites (Sas & Maler, 1983, 1987; Berman & Maler, 1999; Deemyad et al . 2011).…”

“…2018; Metzen et al . 2018). As such, the mechanisms by which serotonergic feedback alters ELL pyramidal cell responses to envelopes most likely differ from those of glutamatergic/GABAergic feedback pathways.…”

Closed-Loop Control of Active Sensing Movements Regulates Sensory Slip

“…For example, rather than relying solely on bottom-up computations, encoding of looming or receding objects is mediated by descending feedback from the midbrain [34]. Similarly, feedback rather than feedforward information processing is involved in extracting electrosensory envelope information, a correlate of distance [46].…”

Behavioral and Neural Aspects of the Spatial Processing of Conspecifics in the Electrosensory System

“…The feedback through nP's stellate cells has also been shown to enhance the response to envelope signals elicited by moving conspecifics (Metzen et al, 2018). The authors of this study showed that the sensitivity of a specific electromotor reaction to the envelope signals of medium to low strength (10-15% contrast) required this input.…”