Adaptation facilitates spatial discrimination for deviant locations in the thalamic reticular nucleus of the rat
Introduction
The auditory environment is continuously filled with concurrent auditory stimuli, yet we can easily isolate and attend to stimuli that are novel or salient. The ability to detect these novel cues is crucial to survival in the ever-changing natural environment, but how does the brain accomplish this task? To answer this question, research has focused on either mismatch negativity (MMN), an event-related potential (ERP) signature in the central nervous system (Näätänen et al., 1978, Näätänen et al., 2007, Aghamolaei et al., 2016), or another putative mechanism for deviant and change detection (Ulanovsky et al., 2003, Yu et al., 2009b): stimulus-specific adaptation (SSA)—when a neuron adapts and even ceases responding to repeated or high-probability stimuli but maintains a comparatively strong response to less common, low-probability stimuli.
Deviance detection within the frequency domain (varying cue tone) has been studied extensively throughout the auditory pathway (Auditory cortex: Ulanovsky et al., 2003, Szymanski et al., 2009, Von Der Behrens et al., 2009, Antunes et al., 2010, Farley et al., 2010, Taaseh et al., 2011, Nieto-Diego and Malmierca, 2016; Medial Geniculate Body: Anderson et al., 2009, Yu et al., 2009b, Antunes et al., 2010, Bäuerle et al., 2011, Antunes and Malmierca, 2014, Duque et al., 2014; Inferior colliculus: Malmierca et al., 2009, Zhao et al., 2011, Ayala and Malmierca, 2012, Ayala and Malmierca, 2015, Ayala et al., 2012, Duque et al., 2012, Duque et al., 2016, Pérez-González et al., 2012, Anderson and Malmierca, 2013). In contrast, much less work has been devoted to the static spatial field (varying cue location). And of those studies that did examine spatial deviants, all of them used artificial closed-field auditory cues exclusively (Reches and Gutfreund, 2008, Xu et al., 2014). Thus, to date no systematic assessment of spatial deviance detection has been carried out at the single neuron level with ecologically relevant stimuli, and as a result, it is still unknown where spatial SSA is represented in the brain.
We hypothesize that the thalamic reticular nucleus (TRN) is critical to spatial SSA. Given its strategic location between thalamus and cortex, TRN has been regarded as the “searchlight of attention” (Crick, 1984, McAlonan et al., 2008). TRN neurons exhibit strong adaptation to repetitive stimuli (Yu et al., 2009a) and show stimulus-specific responses in the frequency domain (Yu et al., 2009b). Neurons in the TRN also show binaural properties (Villa, 1990) and have been related to spatial orienting behavior (Weese et al., 1999). Taken together, the properties of these neurons are consistent with a possible role for the TRN in identifying spatially-novel stimuli. As little is currently known about spatial location processing in the auditory sector of TRN, here we examined spatial SSA in the TRN using in vivo extracellular recordings from both anesthetized and awake rats.
Section snippets
Animals
All animal procedures were approved by the Animal Subjects Ethics Committees of Zhejiang University. Animals were housed in a temperature (24 ± 1 °C) and humidity (40–60%) controlled facility with a 12-h light/12-h dark cycle (lights on at 08:00). Rodent food and water were available ad libitum. Both male and female Wistar rats (260–330 g) with clean external ears were used in the current study.
Anesthesia was induced with 1.35 g/kg urethane (20% solution, i.p., Sinopharm Chemical Reagent Co.,
Results
We recorded from 120 well isolated TRN neurons in 34 anesthetized rats with SOP, and 64 of those were tested with multiple location combinations. We also collected data from 8 neurons in 3 awake rats with one location combination ([−90°, 90°]) in SOP.
Discussion
This study examined spatial SSA of TRN neurons and their spatial discriminability. We found that TRN neurons showed SSA in the spatial domain, and that it was dependent on spatial context. Further, spatial adaptation increased neuronal spatial discriminability for deviant locations by sharpening the response difference (RD) of the two locations.
Conflicts of interest
None.
Author contributions
All authors contributed to the final version of the manuscript. X.X., Y.Z., X.K. and X.Y. designed the experiments, analyzed and interpreted the data; X.X., Y.Z. and X.K. collected and analyzed the data. All authors approved the final version of the manuscript.
Funding
This work was supported by National Natural Science Foundation of China (31671081).
Acknowledgements
We are grateful to Dr. Josef Rauschecker, Dr. Anna Wang Roe, and Dr. Lixia Gao for help with revision of the manuscript.
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