Tactile frequency discrimination is enhanced by circumventing neocortical adaptation

Abstract

Neocortical responses typically adapt to repeated sensory stimulation, improving sensitivity to stimulus changes, but possibly also imposing limitations on perception. For example, it is unclear whether information about stimulus frequency is perturbed by adaptation or encoded by precise response timing. We addressed this question in rat barrel cortex by comparing performance in behavioral tasks with either whisker stimulation, which causes frequency-dependent adaptation, or optical activation of cortically expressed channelrhodopsin-2, which elicits non-adapting neural responses. Circumventing adaption by optical activation substantially improved cross-hemispheric discrimination of stimulus frequency. This improvement persisted when temporal precision of optically evoked spikes was reduced. We were able to replicate whisker-driven behavior only by applying adaptation rules mimicking sensory-evoked responses to optical stimuli. Conversely, in a change-detection task, animals performed better with whisker than optical stimulation. Our results directly demonstrate that sensory adaptation critically governs the perception of stimulus patterns, decreasing fidelity under steady-state conditions in favor of change detection.

Adaptive Processes in Thalamus and Cortex Revealed by Silencing of Primary Visual Cortex during Contrast Adaptation

“…Thus, to understand the neural basis for perception, it is not only necessary to understand how receptive fields change from one stage of processing to the next but also how adaptation cascades along these stages to alter neural response properties depending on the temporal context. This work, plus recent findings in somatosensory cortex [37], demonstrates the utility of optogenetic tools for interrogating these dynamic context-dependent signals. To compare average normalized data, we first equalized dLGN and V1 control curves by shifting both the nonadapted (filled triangles) and adapted (empty triangles) dLGN curves slightly upward so the nonadapted dLGN curve matched the nonadapted V1 curve (filled circles).…”

Cortical Correlates of Low-Level Perception: From Neural Circuits to Percepts

“…In this latter formulation, these circuits are seen as innate building blocks of knowledge for perception that are combined during learning to form complex Lego constructs composed in such a way as to engram new memories (Markram and Perin, 2011). The merit of this bold approach in the rodent is that paradigms developed with primates (see the inspiring work of Bill Newsome and colleagues that linked neurometric and psychometric perceptual measures [Britten et al, 1992]) are now being applied to rodents with measurable success (Bathellier et al, 2012;Musall et al, 2014). But to avoid the trap of nested complexity, it remains necessary to extract generic principles (Marr's algorithmic level) and obtain modeling simplifications.…”

“…Thus, the existence and use of temporal codes may be specific only to some relay stations and pathways, possibly used for specific computations. Recent studies in auditory and somatosensory cortex show a good correlation (Bathellier et al, 2012), possibly even a causal link (Musall et al, 2014;O'Connor et al, 2013), between cortical rate codes and perception. But the simplicity of the stimuli and the behavioral model used in these studies do not exclude the possibility that cortical structures with a high information load such as primate V1 use a sparse code based on precise spike timing, as observed during high-dimensional natural-scene stimulation (Baudot et al, 2013;Vinje and Gallant, 2000).…”

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

“…In a previous study using different frequencies of whisker stimulation for 1 minute, local field potentials and astrocyte somata calcium responses peaked at 5 Hz and decreased at 10 Hz, which they attributed to neuronal adaptation (Wang et al 2006). While we chose to use higher frequencies of stimulation that mimic "stick-slip" events from whisking on textured surfaces, we also limited stimulation to much shorter epochs (1 or 8 s) that reliably produce field potential spikes and calcium transients within neurons (Khatri et al 2004;Musall et al 2014;Mayrhofer et al 2015). During this type of pulsatile whisker stimulation neuronal adaptation occurs within the first few pulses and the number of spikes per pulse decreases, particularly at higher frequencies (Khatri et al 2004;Fraser et al 2006;Musall et al 2014).…”

“…While we chose to use higher frequencies of stimulation that mimic "stick-slip" events from whisking on textured surfaces, we also limited stimulation to much shorter epochs (1 or 8 s) that reliably produce field potential spikes and calcium transients within neurons (Khatri et al 2004;Musall et al 2014;Mayrhofer et al 2015). During this type of pulsatile whisker stimulation neuronal adaptation occurs within the first few pulses and the number of spikes per pulse decreases, particularly at higher frequencies (Khatri et al 2004;Fraser et al 2006;Musall et al 2014). However, neuronal responses remain locked to the pulsatile stimulus (Ewert et al 2008) and are reproducible across many trials (Mayrhofer et al 2015).…”