Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus

Abstract

Serotonin, like other neuromodulators, acts on a range of receptor types, but its effects also depend on the functional characteristics of the neurons responding to receptor activation. In the inferior colliculus (IC), an auditory midbrain nucleus, activation of a common serotonin (5-HT) receptor type, the 5-HT 1A receptor, depresses auditory-evoked responses in many neurons. Whether these effects occur differentially in different types of neurons is unknown. In the current study, the effects of iontophoretic application of the 5-HT 1A agonist 8-OH-DPAT on auditory responses were compared with the characteristic frequencies (CFs), recording depths, and control first-spike latencies of the same group of IC neurons. The 8-OH-DPAT-evoked change in response significantly correlated with first-spike latency across the population, so that response depressions were more prevalent in longer-latency neurons. The 8-OH-DPAT-evoked change in response did not correlate with CF or with recording depth. 8-OH-DPAT also altered the temporal characteristics of spike trains in a subset of neurons that fired multiple spikes in response to brief stimuli. For these neurons, activation of the 5-HT 1A receptor suppressed lagging spikes proportionally more than initial spikes. These results suggest that the 5-HT 1A receptor, by affecting the timing of the responses of both individual neurons and the neuron population, shifts the temporal profile of evoked activity within the IC.

Socially induced serotonergic fluctuations in the male auditory midbrain correlate with female behavior during courtship

“…However, the serotonergic elevations measured in this study are likely to modulate the responses to acoustic stimuli by IC neurons, which express a range of different serotonin receptor types, including receptors in the metabotropic 5-HT1 and 5-HT2 families as well as ionotropic 5-HT3 receptors (Hurley and Sullivan 2012). Activation of different types of serotonin receptors may decrease or increase excitability in the IC by presynaptic or postsynaptic mechanisms (Hurley 2007;Hurley et al 2008;Wang HT et al 2008). One receptor type that is prominently expressed in the IC is the 5-HT1A receptor (Peruzzi andDut 2004, Smith et al 2014;Thompson et al 1994).…”

“…One receptor type that is prominently expressed in the IC is the 5-HT1A receptor (Peruzzi andDut 2004, Smith et al 2014;Thompson et al 1994). Since this receptor type decreases auditory and spontaneous responsiveness and narrows frequency tuning in the IC (Hurley 2006(Hurley , 2007, it may in part account for a prominent effect of exogenously applied serotonin, which is to increase the selectivity of IC neurons for both simple acoustic stimuli and conspecific calls Pollak 2001, 2005). Given the inverse correlation between female rejection behaviors and male serotonergic activity, less rejection from females should be associated with enhanced selectivity for vocalizations.…”

Duration Tuning across Vertebrates

“…Serotonin levels in the IC are modulated by behavioral states (Hurley et al, 2002;Peruzzi and Dut, 2004), and activation of serotonin receptors can shift the FSL of IC neurons (Hurley and Pollak, 2005;Hurley, 2007) and modulate GABAergic inhibition (Hurley et al, 2008). This suggests that behavioral state may modulate the responses of DTNs.…”

Acoustic trauma triggers upregulation of serotonin receptor genes

“…However, the direct comparisons among specific serotonin receptor genes using quantitative PCR in the current study shows that particular receptors show very different magnitudes of upregulation in expression. Because different serotonin receptors have distinct roles in the regulation of excitatory-inhibitory circuitry in the IC (Hurley, 2006; 2007; Hurley et al, 2008; Hurley and Sullivan, 2012), these findings suggest that selective upregulation of receptor expression should be considered part of the suite of specific changes influencing excitatory-inhibitory interactions in the auditory system following hearing loss.…”

“…One such neuromodulatory pathway is the serotonergic system. Different serotonergic receptors regulate excitatory inhibitory circuits in specific ways (Hurley, 2007; Hurley et al, 2008; Hurley and Sullivan, 2012), and neuromodulatory plasticity in this system could differentially influence processing pathways following damage. However, there is a relatively poor understanding of how neuromodulatory receptors regulating particular features of excitatory and inhibitory neurotransmission respond to sensory damage, and whether such responses support adaptive models of sensory plasticity.…”