In a significant new study, Mitra et al.(1) demonstrate the existence of reproducible temporal patterns of spontaneous activity from human functional magnetic resonance imaging (fMRI) recordings. This finding and the novel methods used to demonstrate it bring the question of the role of temporally patterned activity into the domain of human cognition.
The Brain as a Dynamical MachineWhat the brain does is ultimately simple: it takes in sensory information, transforms it into an abstract code of spikes, and uses it to generate motor patterns. This spike code thus constitutes a mental representation of the world, which interacts with memories, expectations, motivations, and other internal states of the animal to generate a series of behaviors that are adaptive and intelligent, and maximize the survival of the individual and the spread of its genes.Incoming information is encoded in all sensory modalities through temporally modulated patterns of activity, with timescales driven by variations in the world and modified by the dynamical properties of sensory receptors. These inputs are filtered, sorted, and integrated into multimodal, task-relevant representations that likely lose their direct temporal correspondence with instantaneous environmental changes. The importance of timing reemerges, however, in the precise choreography of motor output through which different types of motor units are recruited or turned off to generate smooth behavior. Therefore, the brain transforms timed inputs into timed output.It is natural, then, to postulate that the internal code of the brain is also a temporal one, whereby dynamic patterns of action potentials represent the computations that create and manipulate abstract categories. These internal dynamics should serve to modulate and integrate time-varying incoming information. Given that sensory receptors often operate with sensitivity at the physical limit (2, 3), one would expect that any ongoing temporal dynamics should be able to receive and preserve this exquisitely precise information. Such a code could form a common currency for different sensory systems and could be harnessed to, or directly drive, different sets of behavioral outputs. Intuitively, one can therefore imagine that the brain acts as a temporal machine that organizes neuronal activity in time. In fact, the biophysical properties of cortical neurons, with strong nonlinear input-output properties near the action potential threshold, and the fact that most excitatory synapses are weak and depressing, make nonsynchronous activity difficult to propagate (4, 5). One then expects to find series of neurons that fire synchronously but at the same time follow a precise temporal pattern, one that would only be evident in the entire activity of the system. The identification and analysis of these precise firing patterns, and an understanding of how they are implemented in circuits, how they are controlled and modulated, and how they encode represented variables could constitute the "cracking of the neural code."