Population coupling of V1 and V4 neurons and its relation to local cortical state fluctuations and attention in macaque monkey

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Abstract

Neurons couple to various degrees to the activity level of the local neighboring population whereby strongly coupled ‘choristers’ and weakly coupled ‘soloists’ have been identified as two extremes of a continuous spectrum. At the same time neuronal populations undergo coordinated On and Off cortical state activity fluctuations, which are locally modulated by attention. The population coupling of soloists and choristers suggests that soloists should show limited alignment with cortical state fluctuations, while choristers should exhibit profound alignment. To test this, we recorded neurons across cortical layers in macaque areas V1 and V4, while animals performed a feature based spatial attention task. As expected, we found a wide range of population coupling strength of neurons. In line with our prediction, coupling of choristers to cortical state changes (ON-OFF transitions) was generally stronger than that of soloists. The strength of population coupling of neurons was similar during spontaneous and stimulus driven activity. Allocation of attention to the receptive field reduced the population coupling strength. Attentional modulation of neurons was positively correlated with population coupling strength. While neurons on averaged retained their coupling strengths across conditions, some neurons can change coupling strength condition dependent, thereby potentially enhancing the coding abilities of cortical circuits.

Significance statement

Cortical neurons can be categorized according to the level with which they couple their activity to the surrounding population, with extremes being referred to as soloists and choristers, respectively. Here we test to what extent this coupling is a constant feature across cortical states, stimulus and attention conditions. We find that at the population level the coupling is modulated by the conditions under which they are investigated. Critically, individual cells can behave as soloists (or choristers) on average while acting like choristers (soloists) during e.g. cortical state On-Off transitions. Thus, neurons can align with the surrounding population under some conditions, and behave independently under different conditions, thereby potentially enhancing the coding abilities of cortical circuits.

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