Detection of tactile inputs in the rat vibrissa pathway

Abstract

The rapid detection of sensory inputs is crucial for survival. Sensory detection explicitly requires the integration of incoming sensory information and the ability to distinguish between relevant information and ongoing neural activity. In this study, head-fixed rats were trained to detect the presence of a brief deflection of their whiskers resulting from a focused puff of air. The animals showed a monotonic increase in response probability and a decrease in reaction time with increased stimulus strength. High-speed video analysis of whisker motion revealed that animals were more likely to detect the stimulus during periods of reduced self-induced motion of the whiskers, thereby allowing the stimulus-induced whisker motion to exceed the ongoing noise. In parallel, we used voltage-sensitive dye (VSD) imaging of barrel cortex in anesthetized rats receiving the same stimulus set as those in the behavioral portion of this study to assess candidate codes that make use of the full spatiotemporal representation and to compare variability in the trial-by-trial nature of the cortical response and the corresponding variability in the behavioral response. By application of an accumulating evidence framework to the population cortical activity measured in separate animals, a strong correspondence was made between the behavioral output and the neural signaling, in terms of both the response probabilities and the reaction times. Taken together, the results here provide evidence for detection performance that is strongly reliant on the relative strength of signal versus noise, with strong correspondence between behavior and parallel electrophysiological findings.

Response reliability observed with voltage-sensitive dye imaging of cortical layer 2/3: the probability of activation hypothesis

“…Consistent with previous studies, the neural activity started locally over the primary barrel column ϳ10 ms after stimulus presentation (Fig. 1B) and then spread into neighboring barrel columns (Ollerenshaw et al 2012(Ollerenshaw et al , 2014Petersen et al 2003a;Wang et al 2012). In our hands as well as in previous VSD studies, location of the onset of cortical activity is topographic and determined by the identity of the deflected whisker, allowing a direct alignment with the underlying barrel map.…”

“…Images were recorded every 5 ms and the fluorescence quantified as percent change from background. Figure 1B shows trial-average images for six different velocity whisker deflections (V 1 to V 6 ): 75, 150, 300, 600, 900, and 1,200°/s, which span the expected behavioral threshold for detection of the punctate deflection of an individual whisker (Ollerenshaw et al 2012;Stüttgen and Schwarz 2008). Consistent with previous studies, the neural activity started locally over the primary barrel column ϳ10 ms after stimulus presentation (Fig.…”

“…The VSD imaging employed measures population activity in putative cortical layer 2/3 on a single trial with sufficient fidelity as to differentiate stimulusevoked activity on a single stimulus presentation (Ollerenshaw et al 2014). Consistent with previous VSD studies ( Ollerenshaw et al 2012;Petersen et al 2003a) and many decades of trial-averaged electrophysiological evidence, we show that the trial-average amplitude of cortical activation increased with whisker deflection velocity. Despite these trial-average trends, we show that knowledge of trial-average trends was not sufficient to accurately classify response observed on only single trials.…”

“…Behavioral experiments have shown that the probability of detection increases with stimulus velocity (Ollerenshaw et al 2012;Stüttgen and Schwarz 2008), which we observed as an increased probability of response in our VSD signal. A probabilistic behavioral output is matched with a probabilistic neural signal.…”

“…One hypothesis is that sporadic high-velocity "slip-stick" events observed during texture discrimination as a whisker is moved across a surface are relevant stimulus features (Jadhav et al 2009;Wolfe et al 2008). Experiments in our laboratory and others' have shown that both the frequency of stimulus detection in behavioral experiments (Ollerenshaw et al 2012;Stüttgen et al 2006;Stüttgen and Schwarz 2008;Waiblinger et al 2015) and the spike frequency in the thalamus and cortex with extracellular recordings (Boloori et al 2010;Pinto et al 2000;Shoykhet et al 2000;Simons 1978;Wang et al 2010) are modulated by the velocity of the whisker movements. However, neither of these approaches can allow a direct measurement of population response on single trials.…”