Adaptation facilitates spatial discrimination for deviant locations in the thalamic reticular nucleus of the rat

Highlights

• Neurons in the thalamic reticular nucleus exhibited spatial stimulus-specific adaptation.

• Responses at the deviant locations were spatial context dependent.

• Spatial SSA could improve the spatial discriminability for rare locations via sharpening the response gap.

• Strong correlation existed between the adaptation strength and the spatial discrimination for deviant or standard locations.

Abstract

The capacity to identify unanticipated abnormal cues in a natural scene is vital for animal survival. Stimulus-specific adaptation (SSA) has been considered the neuronal correlate for deviance detection. There have been comprehensive assessments of SSA in the frequency domain along the ascending auditory pathway, but only little attention given to deviance detection in the spatial domain. We found that thalamic reticular nucleus (TRN) neurons exhibited stronger responses to a tone when it was presented rarely as opposed to frequently at a certain spatial location. Subsequently, we engaged signal detection theory to directly gauge neuronal spatial discriminability and found that discrimination of deviant locations was considerably higher than standard locations. The variability in neuronal spatial discriminability among the TRN population was directly related to response difference (RD) but not variance; meanwhile, further analyses attributed higher spatial sensitivity at deviant locations to larger RD. Astonishingly, a significant correlation was found between the amount of adaptation and deviant discriminability. Collectively, our results suggest that adaptation facilitates rare location discrimination by sharpening the response gap between two locations.

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.