Offset Responses in the Auditory Cortex Show Unique History Dependence

Abstract

Sensory responses typically vary depending on the recent history of sensory experience. This is essential for processes, including adaptation, efficient coding, and change detection. In the auditory cortex (AC), the short-term history dependence of sound-evoked (onset) responses has been well characterized. Yet many AC neurons also respond to sound terminations, and little is known about the history dependence of these “offset” responses, whether the short-term dynamics of onset and offset responses are correlated, or how these properties are distributed among cell types. Here we presented awake male and female mice with repeating noise burst stimuli while recording single-unit activity from primary AC. We identified parvalbumin and somatostatin interneurons through optotagging, and also separated narrow-spiking from broad-spiking units. We found that offset responses are typically less depressive than onset responses, and this result was robust to a variety of stimulus parameters, controls, measurement types, and selection criteria. Whether a cell's onset response facilitates or depresses does not predict whether its offset response facilitates or depresses. Cell types differed in the dynamics of their onset responses, and in the prevalence, but not the dynamics, of their offset responses. Finally, we clustered cells according to spiking responses and found that response clusters were associated with cell type. Each cluster contained cells of several types, but even within a cluster, cells often showed cell type-specific response dynamics. We conclude that onset and offset responses are differentially influenced by recent sound history, and discuss the implications of this for the encoding of ongoing sound stimuli. SIGNIFICANCE STATEMENT Sensory neuron responses depend on stimulus history. This history dependence is crucial for sensory processing, is precisely controlled at individual synapses and circuits, and is adaptive to the specific requirements of different sensory systems. In the auditory cortex, neurons respond to sound cessation as well as to sound itself, but how history dependence is used along this separate, “offset” information stream is unknown. We show that offset responses are more facilitatory than sound responses, even in neurons where sound responses depress. In contrast to sound onset responses, offset responses are absent in many cells, are relatively homogeneous, and show no cell type-specific differences in history dependence. Offset responses thus show unique response dynamics, suggesting their unique functions.

Sst- and Vip-Cre mouse lines without age-related hearing loss

“…Cre-Lox recombination tools in mice have enabled cell-type specific manipulations of neuronal activity (reviewed in Luo et al, 2018;Taniguchi et al, 2011;Tsien et al, 1996;Zhang et al, 2011) which have provided important insights into circuit mechanisms in the central auditory system (Bigelow et al, 2019;reviewed in DiGuiseppi and Zuo, 2019;Olsen and Hasenstaub, 2022). These tools have revolutionized our understanding of cortical inhibitory interneurons, including the somatostatin (SST) and vasoactive intestinal peptide (VIP) positive cells, which play crucial roles in cortical function (Bigelow et al, 2019;Natan et al, 2015;Pfeffer et al, 2013;Phillips and Hasenstaub, 2016).…”

Omission responses in local field potentials in rat auditory cortex

“…1 A) [ 29 ]. Offset responses can have substantial latencies and durations [ 30 ], and thus could be mistaken for omission responses if their latency coincided with the period of the stimulus train. For this reason, it is important to use a range of stimulus presentation rates when looking for omission responses.…”