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Abstract

Correlated trial-to-trial variability in the activity of cortical neurons is thought to reflect the functional connectivity of the circuit. Many cortical areas are organized into functional columns, in which neurons are believed to be densely connected and share common input. Numerous studies report a high degree of correlated variability between nearby cells. We developed chronically implanted multi-tetrode arrays offering unprecedented recording quality to re-examine this question in primary visual cortex of awake macaques. We found that even nearby neurons with similar orientation tuning show virtually no correlated variability.
In a total of 46 recording sessions from two monkeys, we presented either static or drifting sine-wave gratings at eight different orientations. We recorded from 407 well isolated, visually responsive and orientation-tuned neurons, resulting in 1907 simultaneously recorded pairs of neurons. In 406 of these pairs both neurons were recorded by the same tetrode.
Despite being physically close to each other and having highly overlapping receptive fields, neurons recorded from the same tetrode had exceedingly low spike count correlations (rsc = 0.005 ± 0.004; mean ± SEM). Even cells with similar preferred orientations (rsignal > 0.5) had very weak correlations (rsc = 0.028 ± 0.010). This was also true if pairs were strongly driven by gratings with orientations close to the cells’ preferred orientations.
Correlations between neurons recorded by different tetrodes showed a similar pattern. They were low on average (rsc = 0.010 ± 0.002) with a weak relation between tuning similarity and spike count correlations (two-sample t test, rsignal < 0.5 versus rsignal > 0.5: P = 0.003, n = 1907).
To investigate whether low correlations also occur under more naturalistic stimulus conditions, we presented natural images to one of the monkeys. The average rsc was close to zero (rsc = 0.001 ± 0.005, n = 329) with no relation between receptive field overlap and spike count correlations. We obtained a similar result during stimulation with moving bars in a third monkey (rsc = 0.014 ± 0.011, n = 56).
Our findings suggest a refinement of current models of cortical microcircuit architecture and function: either adjacent neurons share only a few percent of their inputs or, alternatively, their activity is actively decorrelated.