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The Journal of Neuroscience, November 26, 2008, 28(48):12591-12603; doi:10.1523/JNEUROSCI.2929-08.2008

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Behavioral/Systems/Cognitive
Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex

Matthew A. Smith¹ and Adam Kohn^2,3

¹Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, ²Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461, and ³Center for Neural Science, New York University, New York, New York 10003

Correspondence should be addressed to Matthew A. Smith, at his present address: Department of Neuroscience and the Center for the Neural Basis of Cognition, University of Pittsburgh, 4400 Fifth Avenue, Mellon Institute, Room 115, Pittsburgh, PA 15213. Email: masmith{at}cnbc.cmu.edu

The spiking activity of cortical neurons is correlated. For instance, trial-to-trial fluctuations in response strength are shared between neurons, and spikes often occur synchronously. Understanding the properties and mechanisms that generate these forms of correlation is critical for determining their role in cortical processing. We therefore investigated the spatial extent and functional specificity of correlated spontaneous and evoked activity. Because feedforward, recurrent, and feedback pathways have distinct extents and specificity, we reasoned that these measurements could elucidate the contribution of each type of input. We recorded single unit activity with microelectrode arrays which allowed us to measure correlation in many hundreds of pairings, across a large range of spatial scales. Our data show that correlated evoked activity is generated by two mechanisms that link neurons with similar orientation preferences on different spatial scales: one with high temporal precision and a limited spatial extent (3 mm), and a second that gives rise to correlation on a slow time scale and extends as far as we were able to measure (10 mm). The former is consistent with common input provided by horizontal connections; the latter likely involves feedback from extrastriate cortex. Spontaneous activity was correlated over a similar spatial extent, but approximately twice as strongly as evoked activity. Visual stimuli thus caused a substantial decrease in correlation, particularly at response onset. These properties and the circuit mechanism they imply provide new constraints on the functional role that correlation may play in visual processing.

Key words: noise correlation; synchrony; population coding; multielectrode recordings; spontaneous activity; cross-correlogram; signal correlation; array

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Received June 11, 2008; revised Aug. 14, 2008; accepted Oct. 4, 2008.

Correspondence should be addressed to Matthew A. Smith, at his present address: Department of Neuroscience and the Center for the Neural Basis of Cognition, University of Pittsburgh, 4400 Fifth Avenue, Mellon Institute, Room 115, Pittsburgh, PA 15213. Email: masmith{at}cnbc.cmu.edu

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