Serotonergic modulation across sensory modalities

Abstract

The serotonergic system has been widely studied across animal taxa and different functional networks. This modulatory system is therefore well positioned to compare the consequences of neuromodulation for sensory processing across species and modalities at multiple levels of sensory organization. Serotonergic neurons that innervate sensory networks often bidirectionally exchange information with these networks but also receive input representative of motor events or motivational state. This convergence of information supports serotonin's capacity for contextualizing sensory information according to the animal's physiological state and external events. At the level of sensory circuitry, serotonin can have variable effects due to differential projections across specific sensory subregions, as well as differential serotonin receptor type expression within those subregions. Functionally, this infrastructure may gate or filter sensory inputs to emphasize specific stimulus features or select among different streams of information. The near-ubiquitous presence of serotonin and other neuromodulators within sensory regions, coupled with their strong effects on stimulus representation, suggests that these signaling pathways should be considered integral components of sensory systems.

Keywords: auditory system; comparative study; olfactory system; sensory processing; serotonin.

Fig. 1.

Serotonergic modulation of sensory processing. A: intersectional immunohistochemistry using a rabbit polyclonal antibody against serotonin (5-HT, yellow; 1:5,000 dilution; ImmunoStar no. 20080) reveals that serotonergic Drosophila CSDns do not colabel with green fluorescent protein (GFP) expression with a protein-trap transgenic LexA driver for choline acetyltransferase (ChAT, green; BDSC_60319). Neuropil (magenta) delineated with a rat monoclonal antibody against N-cadherin (1:50 dilution; DSHB no. DN-Ex#8). No antibody was used to increase GFP signal. B: intersectional immunohistochemistry reveals that Drosophila CSDns express the 5-HT1B receptor subtype. Here, a protein-trap transgenic GAL4 driver for the 5-HT1B receptor subtype driving the expression of GFP (cyan; the 5-HT1B transgenics were a kind gift from Dr. Herman Dierick, Baylor College of Medicine) colabels with a goat polyclonal antibody against serotonin (yellow; 1:5,000 dilution; ImmunoStar no. 20079). Neuropil (magenta) delineated with a mouse monoclonal antibody against Bruchpilot (1:50 dilution; DSHB no. nc82). A rabbit polyclonal GFP antibody was used to increase GFP signal (1:1,000 dilution; ThermoFisher no. A-11122). C: schematic illustrating general network targets of 5-HT (yellow) highlighted in this review including sensory afferents (purple), local interneurons (orange), in particular presynaptic inhibition, and output neurons (blue). D: 5-HT can alter stimulus intensity coding by shifting the slope of the input-output relationship, modulating response strength, or offsetting the threshold for activation. E: 5-HT can also alter the encoding of stimulus identity by altering tuning breadth or by decreasing spontaneous activity to increase the signal-to-noise ratio. For both A and B, the same immunohistochemistry techniques described in Sizemore and Dacks (2016) were used to collect data. Scale bars, 10 μm.