How do neurons work together? Lessons from auditory cortex

Recordings of single neurons have yielded great insights into the way acoustic stimuli are represented in auditory cortex. However, any one neuron functions as part of a population whose combined activity underlies cortical information processing. Here we review some results obtained by recording simultaneously from auditory cortical populations and individual morphologically identified neurons, in urethane-anesthetized and unanesthetized passively listening rats. Auditory cortical populations produced structured activity patterns both in response to acoustic stimuli, and spontaneously without sensory input. Population spike time patterns were broadly conserved across multiple sensory stimuli and spontaneous events, exhibiting a generally conserved sequential organization lasting approximately 100 ms. Both spontaneous and evoked events exhibited sparse, spatially localized activity in layer 2/3 pyramidal cells, and densely distributed activity in larger layer 5 pyramidal cells and putative interneurons. Laminar propagation differed however, with spontaneous activity spreading upward from deep layers and slowly across columns, but sensory responses initiating in presumptive thalamorecipient layers, spreading rapidly across columns. In both unanesthetized and urethanized rats, global activity fluctuated between "desynchronized" state characterized by low amplitude, high-frequency local field potentials and a "synchronized" state of larger, lower-frequency waves. Computational studies suggested that responses could be predicted by a simple dynamical system model fitted to the spontaneous activity immediately preceding stimulus presentation. Fitting this model to the data yielded a nonlinear self-exciting system model in synchronized states and an approximately linear system in desynchronized states. We comment on the significance of these results for auditory cortical processing of acoustic and non-acoustic information.