Learning speed and detection sensitivity controlled by distinct cortico-fugal neurons in visual cortex.

Sarah Ruediger,Massimo Scanziani

doi:10.7554/elife.59247

Sarah Ruediger, Massimo Scanziani

Open Access

https://doi.org/10.7554/elife.59247

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Abstract

Vertebrates can change their behavior upon detection of visual stimuli according to the outcome their actions produce. Such goal-directed behavior involves evolutionary conserved brain structures like the striatum and optic tectum, which receive ascending visual input from the periphery. In mammals, however, these structures also receive descending visual input from visual cortex (VC), via neurons that give rise to cortico-fugal projections. The function of cortico-fugal neurons in visually guided, goal-directed behavior remains unclear. Here, we address the impact of two populations of cortico-fugal neurons in mouse VC in the learning and performance of a visual detection task. We show that the ablation of striatal projecting neurons reduces learning speed, whereas the ablation of superior colliculus projecting neurons does not impact learning but reduces detection sensitivity. This functional dissociation between distinct cortico-fugal neurons in controlling learning speed and detection sensitivity suggests an adaptive contribution of cortico-fugal pathways even in simple goal-directed behavior.

Highlights

Visual stimuli guide the behavior of many animals
Using an intersectional viral approach to selectively eliminate specific populations of cortico-fugal neurons in visual cortex (VC), we show that the ablation of neurons projecting to the striatum reduces learning speed during task acquisition, whereas the ablation of neurons projecting to the superior colliculus impairs detection sensitivity during task execution
With the area under the ROC curve (aROC) of first lick latencies, it is possible to detect the emergence of visually guided behavior even while hits and false alarms occur at the same rate, as long as the first lick latency in response to a stimulus trial differs from that to a blank trial

Summary

Introduction

Visual stimuli guide the behavior of many animals. While the detection of ethologically relevant visual stimuli can elicit innate behavior, often visual stimuli become relevant through learning, leading to goal-directed behavior upon stimulus detection (Morris et al, 2018; Schultz, 2006). Mammals are able to learn and perform simple sensory detection tasks even in the absence of sensory neocortex (Ceballo et al, 2019; Dalmay et al, 2019; Hong et al, 2018; Poppel et al, 1973; Popper and Fay, 1992; Weiskrantz et al, 1974). It remains unknown whether cortico-fugal pathways, the main output pathways by which VC can influence the rest of the brain and behavior, do contribute to simple goal-directed behavior. These data demonstrate the functional dissociation between two distinct populations of cortico-fugal neurons in VC during specific training stages of a visual detection task and highlight that specific cortico-fugal pathways adaptively contribute even to simple goal-directed behavior

Results

VC lesion CSt ablation

B VGAT-ChR2-YFP pre lesion

Discussion

Materials and methods

Funding Funder NIH