Weak signal amplification and detection by higher-order sensory neurons

Abstract

Sensory systems must extract behaviorally relevant information and therefore often exhibit a very high sensitivity. How the nervous system reaches such high sensitivity levels is an outstanding question in neuroscience. Weakly electric fish (Apteronotus leptorhynchus/albifrons) are an excellent model system to address this question because detailed background knowledge is available regarding their behavioral performance and its underlying neuronal substrate. Apteronotus use their electrosense to detect prey objects. Therefore, they must be able to detect electrical signals as low as 1 μV while using a sensory integration time of <200 ms. How these very weak signals are extracted and amplified by the nervous system is not yet understood. We studied the responses of cells in the early sensory processing areas, namely, the electroreceptor afferents (EAs) and pyramidal cells (PCs) of the electrosensory lobe (ELL), the first-order electrosensory processing area. In agreement with previous work we found that EAs cannot encode very weak signals with a spike count code. However, PCs can encode prey mimic signals by their firing rate, revealing a huge signal amplification between EAs and PCs and also suggesting differences in their stimulus encoding properties. Using a simple leaky integrate-and-fire (LIF) model we predict that the target neurons of PCs in the midbrain torus semicircularis (TS) are able to detect very weak signals. In particular, TS neurons could do so by assuming biologically plausible convergence rates as well as very simple decoding strategies such as temporal integration, threshold crossing, and combining the inputs of PCs.

Synchronous spikes are necessary but not sufficient for a synchrony code in populations of spiking neurons

“…(ii) In courtship contexts the spatial distances between communication partners are low and the signals strong but a mismatch between the signal frequencies and the electroreceptor tuning again leads to weak activation of P-type afferents (20,42,43). (iii) During foraging prey items like the crustacean Daphnia are detected by electric signals created through muscle activity (stimulating the ampullary afferents) and the amplitude modulations induced by their resistive properties (stimulating the P units), which are in the 0.2-1 µV range (44)(45)(46)(47). The weak stimulus regime where a synchrony code is distinct from a simple population code can thus be considered a behaviorally relevant regime in which communication and prey signals need to be encoded and separated from other signals.…”

Electrosensory processing inApteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species

“…To be perceived, stimuli must cause a sufficient change in baseline activity in the first place (Chacron et al 2001;Ratnam and Nelson 2000). While variability in the baseline activity is detrimental for signal detection at the single neuron level (Jung et al 2016), such activity is critical for proper development (Arroyo and Feller 2016;Watt et al 2009). It is, however, likely that such variability is advantageous for coding (McDonnell and Ward 2011;Stein et al 2005).…”

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

“…Mechanisms underlying the ability to detect extremely weak prey stimuli have been identified in weakly electric fish and are likely relevant to the detection of similarly weak conspecific signals. One of the mechanisms identified by Jung et al (2016) relies on a finely balanced inhibition and excitation from feedforward inputs. Balanced inhibition and excitation is a staple feature of many neural networks (e.g.…”

“…These studies point out once again the extreme sensitivity of this system and provide a clear understanding of how these signals are represented at the periphery. The neural mechanisms underlying prey localization and detection are also a good example of sophisticated neural processing strategies used to accomplish challenging tasks (see next section; Clarke, Longtin, & Maler, 2014;Jung, Longtin, & Maler, 2016).…”

“…It was further suggested that prey signals would cause a slight disruption in this patterned receptor spike train and that pyramidal cells could extract this change in pattern (Jung et al, 2016;Nesse, Marsat, Longtin, & Maler, 2012). Although these mechanisms were revealed by focusing on prey capture mechanisms, they are also relevant to the detection of distant conspecific signals and we expect that these concepts will be explored when investigating the mechanisms permitting sensitive conspecific detection and localization.…”