Adaptation to stimulus orientation in mouse primary visual cortex

Abstract

Information processing in the visual system is shaped by recent stimulus history, such that prolonged viewing of an adapting stimulus can alter the perception of subsequently presented test stimuli. In the tilt-after-effect, the perceived orientation of a grating is often repelled away from the orientation of a previously viewed adapting grating. A possible neural correlate for the tilt-after-effect has been described in cat and macaque primary visual cortex (V1), where adaptation produces repulsive shifts in the orientation tuning curves of V1 neurons. We investigated adaptation to stimulus orientation in mouse V1 to determine whether known species differences in orientation processing, notably V1 functional architecture and proportion of tightly tuned cells, are important for these repulsive shifts. Unlike the consistent repulsion reported in other species, we found that repulsion was only about twice as common as attraction in our mouse data. Furthermore, adapted responses were attenuated across all orientations. A simple model that captured key physiological findings reported in cats and mice indicated that the greater proportion of broadly tuned neurons in mice may explain the observed species differences in adaptation.

The speed of neuronal adaptation: A perspective through the visual cortex

“…Historically, shorter durations have been shown to lead to repulsive shifts (Dragoi et al., , ; Hollmann et al., ), whereas, longer adaptation durations have been reported to mainly induce attractive shifts (Ghisovan, Nemri, Shumikhina, & Molotchnikoff, ; Ghisovan et al., ; Jeyabalaratnam et al., ). Notably, the results provided by King and Crowder () confirm the earlier reports that used shorter adaptation durations, but it is important to discuss these results within the context of adaptation durations as they may be central to the type of behavioural response learned by a neuron. It should also be noted that the effects of stimulus size, surround suppression, contrast and spatial frequency have also been studied.…”

“…Had they employed a longer adaptation duration, their results might have changed. However, it should be emphasized that a substantial proportion of attractive shifts in King and Crowder () study may be attributed to (a) end‐of‐flank adaptation, wherein the attractive and repulsive shifts are equally likely, and (b) to salt‐and‐pepper organization of mice cortex, because of which many axes or orientations are active simultaneously in relation to a stimulus, leading to broader tuning curves. As has been modelled by King and Crowder (), such broader tuning curves and the absence of pinwheel centres in mice cortex may lead to both attractive and repulsive shifts.…”

“…However, it should be emphasized that a substantial proportion of attractive shifts in King and Crowder () study may be attributed to (a) end‐of‐flank adaptation, wherein the attractive and repulsive shifts are equally likely, and (b) to salt‐and‐pepper organization of mice cortex, because of which many axes or orientations are active simultaneously in relation to a stimulus, leading to broader tuning curves. As has been modelled by King and Crowder (), such broader tuning curves and the absence of pinwheel centres in mice cortex may lead to both attractive and repulsive shifts. In addition, the effects of adaptation (whether short or long) may even extend to different layers of the cortex as has been demonstrated by Chanauria and colleagues (Chanauria et al., )—that is, layers 2–3 and 5–6 of the primary visual cortex displayed mainly attractive shifts after adaptation, suggesting that such mechanisms may be underlying principles of learning and adaptation at different cortical layers and even areas.…”

“…There have been many contrasting reports in the literature showing the effect of orientation adaptation on visual neurons—the major difference being in the direction of shifts of the peak of orientation selectivity. Some investigations have shown mainly repulsive shifts (Dragoi, Rivadulla, & Sur, ; Dragoi et al., ; Hollmann, Lucks, Kurtz, & Engelmann, ; King & Crowder, ) whereas others have reported primarily attractive shifts (Ghisovan et al., ; Kohn & Movshon, ). However, it is important to note that these studies have employed different adaptation durations (from several seconds to minutes) to change the properties of neurons.…”

“…However, some years back, we showed that, in the primary visual cortex of mouse, adaptation mainly led to attractive shifts (Jeyabalaratnam et al, 2013). In contrast to the study of King and Crowder (2018), we used a longer time interval for the adapter (uninterrupted for 12 min). Historically, shorter durations have been shown to lead to repulsive shifts (Dragoi et al, 2000(Dragoi et al, , 2001Hollmann et al, 2015), whereas, longer adaptation durations have been reported to mainly induce attractive shifts (Ghisovan, Nemri, Shumikhina, & Molotchnikoff, 2008;Ghisovan et al, 2009;Jeyabalaratnam et al, 2013).…”