Widespread presence of direction-reversing neurons in the mouse visual system

Abstract

Direction selectivity -the preference of motion in one direction over the opposite -is a fundamental property of visual neurons across species. We find that a substantial proportion of direction selective neurons in the mouse visual system reverse their preferred direction of motion in response to drifting gratings at different spatiotemporal parameters. A spatiotemporally asymmetric filter model recapitulates our experimental observations.Motion detection is a feature common to all visual animals, and recent work has shown strong parallels in these computations across many species 1-9 . Similar circuits in these animals underlie the comparison of visual information at two locations at two points in time, a computation that establishes direction selectivity wherein a neuron preferentially responds to motion in one direction over its opposite, or null, direction. Here, we report neurons in the mouse visual system that respond preferentially to motion in their null direction at different spatial and temporal frequencies.Using data from the Allen Brain Observatory, a large-scale survey of visual responses in the mouse visual cortex recorded using 2-photon (2P) calcium imaging 10 , we analyzed responses to the drifting grating stimulus. This stimulus consisted of full-field sinusoidal gratings moving in 8 directions and at 5 temporal frequencies (TFs), but at a single spatial frequency (SF). Many neurons showed direction selectivity, and among these direction selective neurons we found some that reverse their direction preference in response to gratings at different TFs (Fig. 1A). We use the direction selectivity index (DSI, see Methods) to quantify the strength of direction selectivity at each TF, fixing the preferred and null directions to those determined at the preferred TF (TF pref , the TF evoking the largest mean response). A negative DSI thus indicates a reversal of direction preference (Fig. 1B, C). We term the neurons exhibiting this phenomenon Direction Reversing Neurons (DRNs).We imposed strict criteria to identify DRNs by comparing their responses at their preferred condition (the preferred direction at TF pref , blue box in Fig. 1A) and reversed condition (the TF at which the neuron has its largest mean response in the null direction, orange box in Fig. 1A). Candidate DRNs must have a DSI ≥ 0.3 for the preferred condition and exhibit a larger response to the null than preferred direction at the reversed condition. These neurons must also pass a strict bootstrap test (see Methods) to ensure the reversal is not a chance observation driven by a small number of outlier trials. 708 out of 12,515 direction selective neurons (6%) met these criteria. Furthermore, we observe DRNs in all visual areas recorded ( Fig. 1D) and across all transgenically defined populations available in the dataset (Fig. SI1).

Complementary inhibitory weight profiles emerge from plasticity and allow attentional switching of receptive fields

“…However, we could substantially alter the responses of the postsynaptic neuron by modulating the activity of either of the two presynaptic inhibitory populations, allowing for the propagation of facets of the input patterns that were previously quenched by inhibition. Such inhibitory modulation can thus serve as a mechanism to selectively filter stimuli according to, e.g., attentional cues, as observed in recent experiments [29][30][31][32][33][34] . In summary, our work proposes a simple biological implementation for an attentional switch of input selectivity, and provides a solution for how such a neuronal circuit can emerge with autonomous and unsupervised, biologically plausible plasticity rules.…”

“…In the framework of our model, such a change in preference could be explained with differential input to the two inhibitory populations, or by changes in their gains through contextual neuromodulation. Similarly, up to 20% of neurons in all areas of the mouse visual system 34 were recently shown to change their preferred orientation according to the (spatial and temporal) frequency of the drifting gratings used in the experiments. These effects could also be explained by temporal fluctuations in the interaction of the two inhibitory populations, and the concurrent changes in transient responses of our model.…”

“…SOM+ interneurons, on the other hand, could follow a non-Hebbian plasticity rule (e.g., anti-Hebbian or homeostatic), which results in a non-selective connectivity 35 . Our second hypothesis posits that changes in the activity of inhibitory neurons are responsible for the highly variable receptive fields observed in recent experiments [29][30][31][32][33][34] (Fig. 1C).…”

“…In macaque V4 31 and V5 32 neurons have been shown to change how they represent different stimuli during detection and discrimination tasks, and in macaque V4 33 some neurons change their hue preference when subjected to single-hue or naturally coloured images. Finally, recent work by Billeh et al 34 showed that in mice, visual neurons change their response to the direction of motion of visual stimuli depending on either the temporal of the spatial frequency of the stimulus (drifting grating). These results suggest that the receptive fields of sensory neurons are dramatically affected by input, context or attentional state, but it is unclear by which mechanisms such changes can transpire.…”

“…To investigate the origins of such varying responses from acquire different synaptic weight profiles after learning that depend on the excitatory weight profile (red dashed line). C, Contextual changes (e.g., due to attention), which we hypothesise to be responsible for modulating the activity of inhibitory populations result in different postsynaptic responses to the same stimulus [29][30][31][32][33][34] , such that preferred (green) and non-preferred (purple) stimuli elicit postsynaptic responses with different amplitudes.…”