Parvalbumin and somatostatin: biomarkers for two parallel tectothalamic pathways in the auditory midbrain

Abstract

The inferior colliculus (IC) represents a crucial relay station in the auditory pathway, located in the midbrain's tectum and primarily projecting to the thalamus. Despite the identification of distinct cell types based on various biomarkers in the IC, their specific contributions to the organization of auditory tectothalamic pathways have remained poorly understood. In this study, we demonstrate that IC neurons expressing parvalbumin (ICPV+) or somatostatin (ICSOM+) represent major, non-overlapping cell types throughout the three IC subdivisions. Strikingly, regardless of their location within the IC, these neurons predominantly project to the primary and secondary auditory thalamic nuclei, respectively. Retrograde tracing data specific to cell types indicate that ICPV+ neurons primarily receive auditory inputs, whereas ICSOM+ neurons integrate polymodal inputs that hold behavioral significance. Furthermore, ICPV+ neurons exhibit significant heterogeneity in both intrinsic electrophysiological properties and presynaptic terminal size compared to ICSOM+ neurons. Notably, approximately one quarter of ICPV+ neurons are inhibitory neurons, whereas all ICSOM+ neurons are excitatory neurons. Collectively, our findings suggest that parvalbumin and somatostatin expression in the IC can serve as biomarkers for two functionally distinct, parallel tectothalamic pathways. This discovery challenges the conventional IC subdivision-based definition of tectothalamic pathways and calls for a reassessment of their functional roles.