Cortical visual processing evokes short-latency reward-predicting cue responses in primate midbrain dopamine neurons

Norihiro Takakuwa,Peter Redgrave,Tadashi Isa

doi:10.1038/s41598-018-33335-9

Abstract

After classical conditioning dopamine (DA) neurons exhibit short latency responses to reward-predicting visual cues. At least two possible projections could induce such DA responses; the cortical and subcortical visual pathways. Our recent study has shown that after a lesion of the striate cortex (V1), the superior colliculus (SC), a critical node of the subcortical visual pathway, can mediate short latency cue responses in the DA neurons of macaque monkeys. An obvious question then is does the cortical pathway have a similar capacity? Using the monkeys with a unilateral V1 lesion that took part in the preceding study, we recorded DA activity while they were performing the same classical conditioning task. However, in this study conditioned visual stimuli were presented to the intact visual field, and the effects of ipsilateral SC inactivation were examined. We found that after the SC was inactivated by injections of muscimol both conditioned behavioral responding and reward-predicting, short latency (~100 ms) cue-elicited DA neuronal responses were unaffected These results indicate that the intact cortical visual pathway can also mediate short latency cue elicited responses in DA neurons in the absence of a normally functioning subcortical visual system.

Highlights

In Pavlovian conditioning, learned associations between sensory stimuli and subsequent rewards or punishments enable animals to engage appropriate anticipatory conditioned responses[1]
The only means of discriminating the conditioned stimuli was the location where they were presented within the visual field
The purpose of the present study was to test whether cortical visual processing can support visual Pavlovian conditioning and evoke short-latency phasic DA responses independently of contribution by the midbrain superior colliculus (SC)

Summary

Introduction

In Pavlovian (classical) conditioning, learned associations between sensory stimuli and subsequent rewards or punishments enable animals to engage appropriate anticipatory conditioned responses[1]. The existence of a direct pathway from the superior colliculus (SC), a critical node in subcortical visual processing, to DA neurons in the ventral midbrain has been demonstrated in a range of mammalian, species including primates[16], rodents[17] and carnivoras[18] This suggests the tecto-nigral projection is a conserved feature of mammalian brain organization, and provides a direct route whereby visual conditioned stimuli can induce short-latency phasic visual responses in ventral midbrain DA neurones[19]. Our previous study[10] begs the question of whether the evolutionary more recent striate visual cortex has the ability to support visual Pavlovian conditioning and evoke short latency phasic activation of DA neurons, independently of the long established subcortical visual processing in the SC To address this issue, we used the same unilaterally V1 lesioned primate preparation[10], except visual conditioned stimuli were presented to the intact cortical visual system, i.e. the visual field contralateral to the intact V1.

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