How do neurons work together? Insights from auditory cortex.
Kenneth D. Harris, Artur Luczak, Peter Bartho, Stephan Marguet, Carina Curto, Shuzo Sakata
Center for Molecular and Behavioral Neuroscience, Rutgers University

The number of spike patterns expressible by even a modest number of neurons is astronomical, particularly if precise spike times, as well as firing rates, are taken into account. In auditory cortex, neural activity can be triggered by sound stimuli, but may also occur spontaneously during silence. We found that both sensory-evoked and spontaneous activity patterns are intricately structured but highly and similarly constrained. Individual neurons responded to stimuli with consistent temporal dynamics, revealing a stereotyped spread of activity across the recorded population. The temporal sequence of neurons firing was quantitatively similar for both spontaneous and evoked events, as well as across different acoustic stimuli, suggesting that the primary difference between responses consisted of the combination of neurons participating in an event, rather than their sequential order. The set of possible neural combinations activated by presentations of any single stimulus was confined to a subset of the set of all possible combinations; the subspaces corresponding to individual stimuli lay within a larger but still constrained realm outlined by the set of spontaneous events. To investigate how such constraints could arise in neural circuits, we constructed a recurrently connected network simulation of diverse excitatory and inhibitory units, which produced similar behavior. Although constraints on spike patterns are inefficient from the point of view of energy efficient coding, we suggest they are an inevitable consequence of information processing in recurrent neuronal networks.